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Human olfaction: a constant state of change-blindness.

Sela L, Sobel N - Exp Brain Res (2010)

Bottom Line: Regarding the temporal envelope, whereas vision and audition consist of nearly continuous input, olfactory input is discreet, made of sniffs widely separated in time.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, The Weizmann Institute of Science, Rehovot, 76100, Israel.

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.

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No time for human olfactory attention. a, b. Results from Youngentob et al. (1987). 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
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Fig3: No time for human olfactory attention. a, b. Results from Youngentob et al. (1987). 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

Mentions: The distal senses of vision, audition, and olfaction differ not only in their ability to produce an internal representation of external space, but also in their temporal envelope. Audition consists of an essentially continuous sampling of the sensory content. Vision similarly entails nearly continuous sampling broken only by occasional blinks, a short lived loss of input on the order of 250 ms (Caffier et al. 2003). Rapid eye movements termed saccades and microsaccades may also entail brief loss of input, although this remains unclear (Burr et al. 1994). In contrast to this largely continuous input in vision and audition, the olfactory system acquires sensory information in temporally discrete quanta, namely sniffs. Olfactory information is made available to the brain during brief bursts followed by often prolonged periods of no input. These bursts are often rhythmic in macrosmatic mammals occurring at between 4 and 11 Hz (Welker 1964; Youngentob et al. 1987), yet are discreet in humans, who tend to use one or very few successive sniffs to explore olfactory content (Laing 1983) (Fig. 3). There has been extensive research on how this unique quantized temporal envelope is reflected in the neural representation of olfaction (Sobel et al. 1998a; Kepecs et al. 2006; Mainland and Sobel 2006; Scott 2006; Verhagen et al. 2007). Here, we suggest that it is also this temporal dynamic that shaped the special place of olfaction in human awareness (awareness in this case refers to the ability of a person to consciously distinguish or detect an olfactory stimulus from the surrounding background). The basis for our claim rests on the phenomena of change blindness. Using vision, humans can detect even the slightest change in the visual scene, and this change detection can function as an orienting cue for attention. Furthermore, changes in a scene are often accompanied by transients such as motion. The motion signal attracts attention to the changed location, and in this way facilitates visual processing (Remington et al. 1992). For example, if one complex landscape image is instantaneously replaced by a second nearly identical landscape image with only one minor change, that change will mostly be detected with ease. Furthermore, visual attention will focus on the change location (Abrams and Christ 2003). However, if a temporal break is introduced between one image and the next, even significant changes in image content may go unnoticed. This phenomenon, termed change blindness (Rensink et al. 1997), can be experienced by the interested reader at several on-line demonstrations (e.g., http://www.psych.ubc.ca/~rensink/flicker/download/). Notably, a similar phenomenon occurs in audition (Vitevitch 2003; Eramudugolla et al. 2005; Wayand et al. 2005; Demany et al. 2008) and touch (Gallace et al. 2006; Auvray et al. 2008) as well. In other words, change blindness (or deafness) suggests that temporal continuity of input is key to awareness. As noted, human olfaction lacks temporal continuity, and therefore we argue that this has dictated a unique, and indeed extremely limited, place for olfaction in human awareness. As this claim is a major point in this review, we will reiterate by example: Look at Fig. 4, then look at a blank page, and then turn the page to look at Fig. 5. Do this such that the transition from Figs. 4, 5 takes a few seconds. Can you detect the change between figures? Such is human olfaction. A slow transition from one image (sniff) to the next, with a blank page inserted in between. Although change blindness may differ from the case of olfaction in that it requires an intentional search of the change in the scene, other features of change blindness, namely the inability to detect change in quantal as opposed to continuous information, provides a powerful analogy to the constant state of olfaction.Fig. 3


Human olfaction: a constant state of change-blindness.

Sela L, Sobel N - Exp Brain Res (2010)

No time for human olfactory attention. a, b. Results from Youngentob et al. (1987). 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
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Related In: Results  -  Collection

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Fig3: No time for human olfactory attention. a, b. Results from Youngentob et al. (1987). 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
Mentions: The distal senses of vision, audition, and olfaction differ not only in their ability to produce an internal representation of external space, but also in their temporal envelope. Audition consists of an essentially continuous sampling of the sensory content. Vision similarly entails nearly continuous sampling broken only by occasional blinks, a short lived loss of input on the order of 250 ms (Caffier et al. 2003). Rapid eye movements termed saccades and microsaccades may also entail brief loss of input, although this remains unclear (Burr et al. 1994). In contrast to this largely continuous input in vision and audition, the olfactory system acquires sensory information in temporally discrete quanta, namely sniffs. Olfactory information is made available to the brain during brief bursts followed by often prolonged periods of no input. These bursts are often rhythmic in macrosmatic mammals occurring at between 4 and 11 Hz (Welker 1964; Youngentob et al. 1987), yet are discreet in humans, who tend to use one or very few successive sniffs to explore olfactory content (Laing 1983) (Fig. 3). There has been extensive research on how this unique quantized temporal envelope is reflected in the neural representation of olfaction (Sobel et al. 1998a; Kepecs et al. 2006; Mainland and Sobel 2006; Scott 2006; Verhagen et al. 2007). Here, we suggest that it is also this temporal dynamic that shaped the special place of olfaction in human awareness (awareness in this case refers to the ability of a person to consciously distinguish or detect an olfactory stimulus from the surrounding background). The basis for our claim rests on the phenomena of change blindness. Using vision, humans can detect even the slightest change in the visual scene, and this change detection can function as an orienting cue for attention. Furthermore, changes in a scene are often accompanied by transients such as motion. The motion signal attracts attention to the changed location, and in this way facilitates visual processing (Remington et al. 1992). For example, if one complex landscape image is instantaneously replaced by a second nearly identical landscape image with only one minor change, that change will mostly be detected with ease. Furthermore, visual attention will focus on the change location (Abrams and Christ 2003). However, if a temporal break is introduced between one image and the next, even significant changes in image content may go unnoticed. This phenomenon, termed change blindness (Rensink et al. 1997), can be experienced by the interested reader at several on-line demonstrations (e.g., http://www.psych.ubc.ca/~rensink/flicker/download/). Notably, a similar phenomenon occurs in audition (Vitevitch 2003; Eramudugolla et al. 2005; Wayand et al. 2005; Demany et al. 2008) and touch (Gallace et al. 2006; Auvray et al. 2008) as well. In other words, change blindness (or deafness) suggests that temporal continuity of input is key to awareness. As noted, human olfaction lacks temporal continuity, and therefore we argue that this has dictated a unique, and indeed extremely limited, place for olfaction in human awareness. As this claim is a major point in this review, we will reiterate by example: Look at Fig. 4, then look at a blank page, and then turn the page to look at Fig. 5. Do this such that the transition from Figs. 4, 5 takes a few seconds. Can you detect the change between figures? Such is human olfaction. A slow transition from one image (sniff) to the next, with a blank page inserted in between. Although change blindness may differ from the case of olfaction in that it requires an intentional search of the change in the scene, other features of change blindness, namely the inability to detect change in quantal as opposed to continuous information, provides a powerful analogy to the constant state of olfaction.Fig. 3

Bottom Line: Regarding the temporal envelope, whereas vision and audition consist of nearly continuous input, olfactory input is discreet, made of sniffs widely separated in time.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, The Weizmann Institute of Science, Rehovot, 76100, Israel.

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.

Show MeSH
Related in: MedlinePlus