Olfaction in Action
Year: 2009
Type: dissertation
Abstract: Recent evidence has contributed to change the view according to which action representation chiefly depends on visual information. In particular, research on hand grasping actions has emphasized that a multimodal interplay across vision, audition, the sense of touch, and proprioception occurs when performing and understanding an action (e.g., Castiello, 1996; Patchay, Castiello, & Haggard, 2003; Gazzola, Aziz-Zadeh, & Keysers, 2006; Zahariev & MacKenzie, 2007). The experimental work included in the present thesis aimed at extending the multisensory aspects of action representation to the olfactory domain. I first addressed this issue from the perspective of action execution by asking participants to reach and grasp a target-object under different circumstances of visual and olfactory stimulation. The angular excursion at the level of individual digits, digits’ angular distance, and arm movement duration were recorded. Next, I focused on action understanding by asking participants to observe others’ grasping actions under different visual and olfactory conditions. Here, cerebral activity of the neural system responsible for action understanding, i.e., the Action Observation System (AOS) was recorded. An overview of this experimentation is outlined in the following section. OVERVIEW OF THE PRESENT RESEARCH In the first two experiments (Thesis Chapters 3 and 4) participants were requested to reach towards and grasp either a small or a large visual target calling for different types of grasp, precision grip (PG) and whole hand grasp (WHG), respectively. This task was performed in the absence or in the presence of an odour associated with objects that, if grasped, would require a PG or a WHG. The aim of these experiments was twofold. First, to understand whether the central nervous system (CNS) can use olfactory information to select and execute a ‘grasp’ motor plan. Second, to shed light on how detailed the motor commands embedded within the ‘grasp’ plans elicited by an object’s olfactory representation are. The results showed that merely smelling the odour associated with a small and a large object activates the kinematic parameterization of the action appropriate for grasp that object, i.e., PG and WHG, respectively. Therefore, the CNS is able to convert the geometric features of an olfactory-encoded object (e.g., size) into the motor prototype for interacting with that object. In other words, the visuomotor mechanism underlying the control of action (e.g., Castiello, 1996) appears to be sensitive to olfactory information. From a perceptual perspective, the representation evoked by the odour seems to contain highly detailed information regarding the object (i.e., volumetric features). This is because the effect of odour ‘size’ was played out on the hand posture at the level of individual digits’ motion. If olfaction had provided a blurred and holistic object’s representation (i.e., a low spatial-resolution of the object’s image), then the odour would have not affected would have not affected the hand in its entirety. From a motor perspective, the olfactory representation seems to be mapped into the action vocabulary with a certain degree of reliability. The elicited motor plan is not an incomplete primal sketch which only provides a preliminary descriptive in the terms of motor execution but it embodies specific and selective commands for handling the ‘smelled’ object. In the experiments described above the odour associated with the object was always delivered before movement initiation and before the target became visually available. For the motor control system this entailed to prioritize the ‘olfactory’ non-target object with respect to the visual target. Specifically, planning and execution of action was first based on the sense of smell. In this respect, previous research on grasping actions revealed that visual nontarget-objects do not activate the corresponding ‘grasp’ plans when prior knowledge regarding the visual target is given to participants (e.g., Castiello, 1996). In order to investigate whether this caveat also applies for nontarget-objects signalled via olfaction, I performed an experiment (Thesis Chapters 5) similar to those reported above, but participants were given sufficient time to code for the visual target before movement initiation. The results showed that in such circumstances the odour ‘size’ did modulate the temporal organization of the arm movement. Therefore, even when olfactory information plays a secondary role with respect to visual information for action guidance, the olfactory-encoded object is represented within the motor system. And, traces of the ‘grasp’ motor plan associated with the olfactory object remain evident at the level of the arm movement. Having demonstrated the influence that olfactory stimuli might have for the control of action I reasoned that such phenomenon might be relevant for investigating possible gender differences in the use of olfactory information within the action domain (e.g., Ecuyer-Dab & Robert, 2004). Therefore by using an experimental paradigm similar to that reported in Thesis Chapter 4, I investigated whether gender differences were evident when odours of objects had to be mapped into the corresponding ‘grasp’ motor plans (Thesis Chapter 6). The results showed that for men arm-movement duration increased when the ‘size’ of the odour did not match the size of the visual target. Whereas, for women such effect was not revealed. Remember that a lengthening in movement duration was taken as evidence for an odour-induced activation of the ‘grasp’ motor plans associated with the ‘smelled-objects’ (Thesis Chapter 4). Therefore, it appears that male sense of smell is action-oriented, i.e., tailored to elicit specific and selective motor commands for act upon olfactory-encoded objects. Whereas, in line with previous evidences stemming from research on human olfaction, the female sense of smell would be perception-oriented, i.e., optimised to detect, discriminate, identify, recognise, and categorise odours (e.g., Brand & Millot, 2001). Once documented that the sense of smell provides useful information for planning and execute an action I investigated whether olfactory cues may also contribute to the understanding of others’ actions. The fMRI experiment reported in Thesis Chapter 7 was conceived to specifically address this issue. The results showed that the neural system devoted to action understanding (i.e., the ASO) represented both a hand grasping an ‘olfactory’ object and a mimed hand grasp. Importantly, evidence that the AOS was also able to differentiate between these two type of actions was also found. The discrimination process might solely be ascribed to the olfactory information which signalled the target-object. Therefore, the role played by olfactory information in action understanding was demonstrated. With this in mind the central advance of the present work is twofold. First, I demonstrated that processes of selection for the control of actions may be based on olfactory information. This was done by linking current advances in the methodology for recording hand kinematics and paradigms considering the presence of nontarget-object. Second, I provided evidence for the contribution of olfactory information to the understanding of other’s actions. This was achieved by combining the fMRI technique with an action observation paradigm. REFERENCES Brand, G., & Millot, J. L. (2001). Sex differences in human olfaction: between evidence and enigma. Quarterly Journal of Experimental Psychology, 54, 259-270. Castiello, U. (1996). Grasping a fruit: selection for action. Journal of Experimental Psychology: Human Perception and Performance, 22, 582-603. Ecuyer-Dab, I., & Robert, M. (2004). Have sex differences in spatial ability evolved from male competition for mating and female concern for survival? Cognition, 91, 221-257. Gazzola, V., Aziz-Zadeh, L., & Keysers, C. (2006). Empathy and the somatotopic auditory mirror system in humans. Current Biology, 16, 1824-1829. Patchay, S., Castiello, U., & Haggard, P. (2003). A crossmodal interference effect in grasping objects. Psychological Bulletin Reviews, 10, 924-931. Zahariev M. A., & MacKenzie, C. L. (2007) Grasping at thin air: multimodal contact cues for reaching and grasping. Experimental Brain Research, 180, 69-84.
Author: Federico Tubaldi
Language: English
Subfield: Social Psychology
Field: Psychology
Domain: Social Sciences
Open Access status: green
OpenAlex ID: W67394003