Similar to binocular rivalry [17
], the binaral competition observed here is related to adaption. In Experiment 2, when one nostril was adapted for 2mins to PEA, and then the same nostril was again presented with PEA while the other nostril was presented with n-butanol, subjects (N = 4) reported smelling the ‘marker’ smell. Conversely, when one nostril was pre-adapted to n-butanol, and then the same nostril was again presented with n-butanol while the other nostril was presented with PEA, the same subjects reported smelling the ‘rose’ smell. Nevertheless, Experiment 2 does not tell us whether the contribution of adaptation is due to central (adaptation occurred in the cortex) or peripheral (adaptation occurred at the peripheral receptor neurons) components.
As a preparatory step towards addressing this issue, we examined the effect of adaptation on the perceived intensity of the odorants in Experiment 3. Subjects were adapted for 2mins to an odorant in one nostril, and then rated the perceived intensity of the same adapting odorant or a different odorant in either the same or the other nostril. As would be expected from adaptation, when either PEA or n-butanol was presented to the nostril that had been pre-adapted to it, it was rated as much less intense [t (11) = −4.64, p = 0.001] than before the adaptation (). One interesting question is whether such adaptation is purely peripheral, i.e. only due to the fatigue of the peripheral olfactory receptor neurons over prolonged exposure to the odorant. We find this not to be the case. When the same odorant was presented to the other nostril, which had not been adapted to it, there was also a significant drop of its intensity rating [t (11) = −3.57, p = 0.004]; although the effect is less drastic as compared to when it was presented to the pre-adapted nostril [t (11) = −2.66, p = 0.022]. Hence both cortical and peripheral mechanisms are involved, as previously demonstrated by Cain [18
]. This adaption is odorant-specific. The intensity rating of the odorant (n-butanol or PEA) that had not been adapted to was not affected [t (11) = −0.74 and −1.63, p = 0.47 and 0.13, respectively, for the two nostrils] ().
Figure 2 Olfactory adaptation consists of both cortical and peripheral components. Since there was no significant effect of adapting side [F (1, 11) = 0.40, p = 0.54], adapting odorant [F (1, 11) = 0.55, p = 0.47], testing side [F (1, 11) = 0.004, p = 0.95], or (more ...)
Subsequently in Experiment 4 and 5, we set forth to assess whether both cortical adaptation and adaptation of the olfactory receptors contribute to the alternations in olfactory percepts observed in Experiment 1. We hypothesized that if cortical adaptation is an important component of binaral rivalry, alternating olfactory percepts would be experienced independent of adaptation in the olfactory epithelium (mononaral rivalry) (Experiment 4), as in monocular rivalry [19
]. Indeed, ten out of the twelve subjects (83%) experienced switches between smelling predominantly ‘rose’ and smelling predominantly ‘marker’ when they intermittently sampled from two bottles, each containing a 1:1 mixture (8ml) of PEA (0.5% in propylene glycol, 4ml) and n-butanol (0.5% in propylene glycol, 4ml) ( and Table S1
). On average, for the same individual, the percepts altered from a maximum of 70% like ‘rose’ to a maximum of 78.7% like ‘marker’. Across the 12 subjects, the similarity ratings ranged from 90% like ‘rose’ to 92% like ‘marker’. Similar to the aforementioned binaral rivalry situation, subjects experienced a decrease in the intensity of the perceived smell [F (19, 209) = 2.19, p = 0.004] over time. Their pleasantness ratings, again significantly correlated with the similarity ratings across subjects [average r = 0.44, s.e.m. = 0.11, t (11) = 3.94, p = 0.002], were not affected by the number of times the odorants were sampled [F (19, 209) = 1.11, p = 0.35].
Figure 3 Mononaral rivalry. Ten out of the twelve subjects tested experienced switches between perceiving predominantly ‘rose’ and predominantly ‘marker’ (y-axis, similarity rating to ‘rose’ or ‘marker’ (more ...)
Concerning the peripheral adaptation at the olfactory epithelium, we hypothesized that if it also plays a significant role in binaral rivalry, a swap of the sides of the two olfactory stimuli would render the previously suppressed smell perceivable again (in parallel to what is observed in binocular rivalry [20
]). To test this idea, in Experiment 5, subjects were instructed to simultaneously and continuously sniff from two bottles, one containing PEA (0.5% in propylene glycol, 8ml) and the other containing n-butanol (0.5% in propylene glycol, 8ml), until they can no longer detect the smell they firstly did (e.g. if a subject firstly smelled ‘marker’, he was instructed to keep sniffing until he did not smell the ‘marker’ smell). Then unknown to the subjects, the two bottles were either quickly swapped or not swapped and re-presented to the two nostrils. Consistent with our hypothesis, ten out of the twelve subjects tested (83%) reported smelling the same smell again (e.g. marker) when the bottles were swapped, but not when the bottles were not swapped.
It is worth noting that although the mononaral rivalry (Experiment 4) resembles binaral rivalry (Experiment 1) in perceptual experience ( & ), the two recruit different mechanisms. Whereas mononaral rivalry is independent of adaptation in the olfactory epithelia located in the two nostrils (Experiment 4), there is a significant peripheral component in binaral rivalry, as shown in Experiment 5. These results are consistent with what has been found in visual rivalry [22
In the visual system, inhibitory interactions could take place among both monocular neurons (binocular/interocular competition) and binocular pattern-selective neurons (monocular/pattern competition), and the persisting neural signals could be passed on to higher stages of processing, where visual competition can continue [2
]. Anatomical parallel exists between the olfactory system and the visual system. Olfactory system is largely ipsilateral [24
]. Odorants entering one nostril is detected by the olfactory epithelium, from which the olfactory information is conducted to the ipsilateral olfactory bulb. Axons of the mitral and tufted cells of each bulb coalesce and form the olfactory tract, one on each side, which conveys olfactory information ipsilaterally to the primary olfactory cortex (anterior olfactory nucleus, olfactory tubercle, anterior and posterior piriform cortex, amygdala, and rostral entorhinal cortex). There is inhibitory interaction between the two olfactory bulbs [25
]. In addition, there is inhibitory interaction among olfactory bulb glomeruli [26
], which receive olfactory inputs from different types of odorant receptors [27
]. The two olfactory tracts are nevertheless connected to each other via the anterior olfactory nuclei and the anterior commissure [28
]. Such anatomical substrates possibly contribute to the binaral and mononaral rivalries observed here, yet the neural mechanisms of olfactory rivalry await to be elucidated.