Commentary: Cortical plasticity and olfactory function in early blindnes

Fiore, Alessandra

Pazzaglia, Mariella

Frontiers in Human Neuroscience

English

PubMed

Alessandra Fiore

Mariella Pazzaglia

Crossref

Commentary: Cortical Plasticity and Olfactory Function in Early Blindness

Frontiers - Publisher Connector

GENERAL COMMENTARY
published: 09 January 2017
doi: 10.3389/fnhum.2016.00689
Frontiers in Human Neuroscience | www.frontiersin.org 1 January 2017 | Volume 10 | Article 689
Edited by:
Stephane Perrey,
University of Montpellier, France
Reviewed by:
Tao Zhang,
Institute of Biotechnology (CAS),
China
*Correspondence:
Mariella Pazzaglia
mariella.pazzaglia@uniroma1.it
Received: 19 October 2016
Accepted: 26 December 2016
Published: 09 January 2017
Citation:
Fiore A and Pazzaglia M (2017)
Commentary: Cortical Plasticity and
Olfactory Function in Early Blindness.
Front. Hum. Neurosci. 10:689.
doi: 10.3389/fnhum.2016.00689
Commentary: Cortical Plasticity and
Olfactory Function in Early Blindness
Alessandra Fiore 1 and Mariella Pazzaglia 1, 2*
1Department of Psychology, University of Rome “La Sapienza”, Rome, Italy, 2 IRCCS Santa Lucia Foundation, Rome, Italy
Keywords: olfactory, visual, plasticity, multimodal integration, rehabilitation, motor activity
A commentary on
Cortical Plasticity and Olfactory Function in Early Blindness
by Araneda, R., Renier, L. A., Rombaux, P., Cuevas, I., and De Volder, A. G. (2016). Front. Syst.
Neurosci. 10:75. doi: 10.3389/fnsys.2016.00075
Humans beings are visual creatures, which means that they preferentially map the world guided
largely by sight (Aglioti and Pazzaglia, 2010). However, multiple senses contribute to the creation
of an integrated experience of the real world (Aglioti and Pazzaglia, 2011). Among these, the
olfactory sense is undoubtedly the most neglected. One of the reasons for this is that odors do
not always prevail at a conscious level (Sobel et al., 1999), even though olfactory receptors are
continuously active in order to acquire sensory, motor and affective information (Pazzaglia, 2015).
A second reason is the fact that sight occasionally prevails over, or even hides, the information
provided by other senses. In a recent stimulating and timely article, Araneda and colleagues
presented an important view of the pathophysiological mechanisms of plasticity that occur in
the visual brain of early blind patients (Araneda et al., 2016). The authors produced a behavioral
and anatomo-physiological perspective on the guiding role of olfactory information when sight is
lacking. Behaviorally, early blind subjects perform better than sighted individuals when it comes
to odor detection and awareness, indicating that the sense of smell is highly plastic and suggesting
the possibility of incremental odor processing by way of learning and experience. Neurally, active
olfactory processing occurs within the occipital cortex, suggesting the privileged access of odor to
other, seemingly unrelated, sensory systems and neural regions.
The study of Araneda and colleagues also provides an excellent opportunity to investigate
olfactory information, not only in the complete absence of visual mediation (e.g., in congenitally
blind individuals), but also in terms of understanding the value of this extraordinary plasticity
in relation to the enhanced olfactory abilities of many of our sensations, perceptions, and
higher-order cognitive processing. This is an important topic, and the contribution of cross-modal
visual-olfactory interaction can certainly be emphasized, as this is supported by much experimental
evidence in terms of highlighting the implications in the field of clinical studies. The congruent
odor of an object facilities how it is visually represented (Verhagen and Engelen, 2006), and
the concurrent presence of the visual cues of a given object may also enhance olfactory
performances (Gottfried and Dolan, 2003). The relevance of olfaction in visual areas has been
demonstrated in a causative study using repetitive transcranial magnetic stimulation, which showed
that olfactory performances improve when occipital areas in the brain are stimulated, even in
seeing humans (Jadauji et al., 2012). The merging of a visual representation enables healthy
individuals to optimize their identification and discrimination of an object based on smell alone.
Analogously, neuroimaging studies have reported modulation in visual cortices during purely
olfactory performances (Qureshy et al., 2000; Zatorre et al., 2000; Dade et al., 2002), hinting at
genuine cross-modal neural modulation evoked by olfactory cues. In addition to conveying visual
information, it is known that odors also trigger more dynamic information about visual motor
states (Kuang and Zhang, 2014).
Fiore and Pazzaglia Smelling Visual Objects, Actions and Worlds
The merging of visual and olfactory information facilitates
the kinematics of reach-to-grasp movements and understanding
actions (Tubaldi et al., 2011). When a person observes someone
else grasping an object, the neurons that control the hand
muscles in the observer become more alert, as if the individual
is also preparing to perform the same action (Fadiga et al.,
1995). If someone smells the aroma of a strawberry while
simultaneously observing someone else grasping this fruit, the
olfactory information activates in the observer the brain regions
involved in the congruent body movements (Rossi et al., 2008).
This facilitation effect of olfaction on movement parameters
is specific to the muscles that guide the observed movement
(Castiello, 1997). Conversely, the perception of smelling a
different food (orange) object did not induce any facilitation of
the corticospinal system.
Clinically, being driven by visual-olfactory inputs to the
mapping of actions could assuage motor disturbances. In
Parkinson’s disease (PD), for example (Castiello et al., 2009;
Parma et al., 2013a), patients present, among other symptoms,
with an impairment of the kinematics of movements. Like
healthy subjects, a clear facilitation with the kinematics of
reaching and grasping movements was found in patients with
PD in conditions of coherent actions between the object and
odor. This suggests that cross-modal processing optimizes, not
only perceptive, but also motor, functioning. Nevertheless, in
clinical applications, the imitation of reach-to-grasp movements
has been facilitated in a condition paired with the smell of
the subject’s own mother in Autism Spectrum Disorder (ASD)
(Parma et al., 2013b). The smell of a stranger did not, however,
modulate automatic visual-motor actions. Accordingly, a familiar
body odor may promote socio-cognitive behavior such as the
spontaneous imitation that is impaired in ASD. Together, these
studies show that the olfactory modality may interact with
visual-motor behavior in clinical and healthy populations in
order to integrate perceptions that, ultimately, may appear to
be exclusively visual (Pazzaglia et al., 2016). The mechanism
through which the visual and motor system is connected to
higher-order olfactory perception is worth investigating, and
could have important clinical applications. Olfaction is probably
interacting with vision in multiple pathways. Olfactory sources
for building integrated multisensory perceptions can develop
very rapidly for perceiving and interacting with objects and
actions. The actions triggered by the smelling source indicate that
olfactory cues may implicitly predict and trigger action planning
(Pazzaglia, 2013; Pazzaglia and Galli, 2015). These interesting
possibilities await further research before this could become a
useful tool in clinics. Consequently, by exploring how a greater
use of odorous stimuli contributes to visual and motor planning
remains a fundamental application in a clinical perspective (Galli
et al., 2015; Galli and Pazzaglia, 2015; Pazzaglia and Molinari,
2016). The functional gain derived from odor integration might
optimize rehabilitation programmes in case of generalized motor
impairment and disturbed human social interaction.
AUTHOR CONTRIBUTIONS
All authors listed, have made substantial, direct and intellectual
contribution to the work, and approved it for publication.
REFERENCES
Aglioti, S. M., and Pazzaglia, M. (2010). Representing actions through their sound.
Exp. Brain Res. 206, 141–151. doi: 10.1007/s00221-010-2344-x
Aglioti, S.M., and Pazzaglia,M. (2011). Sounds and scents in (social) action.Trends
Cogn. Sci. 15, 47–55. doi: 10.1016/j.tics.2010.12.003
Araneda, R., Renier, L. A., Rombaux, P., Cuevas, I., and De Volder, A. G. (2016).
Cortical Plasticity and Olfactory Function in Early Blindness. Front. Syst.
Neurosci. 10:75. doi: 10.3389/fnsys.2016.00075
Castiello, U. (1997). Arm and mouth coordination during the eating
action in humans: a kinematic analysis. Exp. Brain Res. 115, 552–556.
doi: 10.1007/PL00005726
Castiello, U., Ansuini, C., Bulgheroni, M., Scaravilli, T., and Nicoletti, R. (2009).
Visuomotor priming effects in Parkinson’s disease patients depend on the
match between the observed and the executed action. Neuropsychologia 47,
835–842. doi: 10.1016/j.neuropsychologia.2008.12.016
Dade, L. A., Zatorre, R. J., and Jones-Gotman, M. (2002). Olfactory learning:
convergent findings from lesion and brain imaging studies in humans. Brain
125, 86–101. doi: 10.1093/brain/awf003
Fadiga, L., Fogassi, L., Pavesi, G., and Rizzolatti, G. (1995). Motor facilitation
during action observation: a magnetic stimulation study. J. Neurophysiol. 73,
2608–2611.
Galli, G., Lenggenhager, B., Scivoletto, G., Molinari, M., and Pazzaglia, M. (2015).
Don’t look at my wheelchair! The plasticity of longlasting prejudice.Med. Educ.
49, 1239–1247. doi: 10.1111/medu.12834
Galli, G., and Pazzaglia, M. (2015). Commentary on: “The body social: an enactive
approach to the self.” A tool for merging bodily and social self in immobile
individuals. Front. Psychol. 6:305. doi: 10.3389/fpsyg.2015.00305
Gottfried, J. A., and Dolan, R. J. (2003). The nose smells what the eye sees:
crossmodal visual facilitation of human olfactory perception. Neuron 39,
375–386. doi: 10.1016/S0896-6273(03)00392-1
Jadauji, J. B., Djordjevic, J., Lundstrom, J. N., and Pack, C. C. (2012). Modulation
of olfactory perception by visual cortex stimulation. J. Neurosci. 32, 3095–3100.
doi: 10.1523/JNEUROSCI.6022-11.2012
Kuang, S., and Zhang, T. (2014). Smelling directions: olfaction modulates
ambiguous visual motion perception. Sci. Rep. 4, 5796. doi: 10.1038/srep05796
Parma, V., Bulgheroni, M., Scaravilli, T., Tirindelli, R., and Castiello, U. (2013a).
Implicit olfactory processing attenuates motor disturbances in idiopathic
Parkinson’s disease. Cortex 49, 1241–1251. doi: 10.1016/j.cortex.2012.05.017
Parma, V., Bulgheroni, M., Tirindelli, R., and Castiello, U. (2013b). Body
odors promote automatic imitation in autism. Biol. Psychiatry 74, 220–226.
doi: 10.1016/j.biopsych.2013.01.010
Pazzaglia, M. (2013). Does what you hear predict what you will do and say? Behav.
Brain Sci. 36, 370–371. doi: 10.1017/S0140525X12002804
Pazzaglia, M. (2015). Body and odors: non just molecules, after all. Curr. Dir.
Psychol. Sci. 24, 329–333. doi: 10.1177/0963721415575329
Pazzaglia, M., and Galli, G. (2015). Translating novel findings of perceptual-motor
codes into the neuro-rehabilitation of movement disorders. Front. Behav.
Neurosci. 9:222. doi: 10.3389/fnbeh.2015.00222
Pazzaglia, M., Haggard, P., Scivoletto, G., Molinari, M., and Lenggenhager, B.
(2016). Pain and somatic sensation are transiently normalized by illusory body
ownership in a patient with spinal cord injury. Restor. Neurol. Neurosci. 34,
603–613. doi: 10.3233/RNN-150611
Pazzaglia, M., and Molinari, M. (2016). The embodiment of assistive
devices-from wheelchair to exoskeleton. Phys. Life Rev. 16, 163–175.
doi: 10.1016/j.plrev.2015.11.006
Frontiers in Human Neuroscience | www.frontiersin.org 2 January 2017 | Volume 10 | Article 689
Fiore and Pazzaglia Smelling Visual Objects, Actions and Worlds
Qureshy, A., Kawashima, R., Imran, M. B., Sugiura, M., Goto, R., Okada, K., et al.
(2000). Functional mapping of human brain in olfactory processing: a PET
study. J. Neurophysiol. 84, 1656–1666.
Rossi, S., De Capua, A., Pasqualetti, P., Ulivelli, M., Fadiga, L., Falzarano, V., et al.
(2008). Distinct olfactory cross-modal effects on the human motor system.
PLoS ONE 3:e1702. doi: 10.1371/journal.pone.0001702
Sobel, N., Prabhakaran, V., Hartley, C. A., Desmond, J. E., Glover, G. H., Sullivan,
E. V., et al. (1999). Blind smell: brain activation induced by an undetected
air-borne chemical. Brain 122(Pt 2), 209–217. doi: 10.1093/brain/122.2.209
Tubaldi, F., Turella, L., Pierno, A. C., Grodd, W., Tirindelli, R., and Castiello,
U. (2011). Smelling odors, understanding actions. Soc. Neurosci. 6, 31–47.
doi: 10.1080/17470911003691089
Verhagen, J. V., and Engelen, L. (2006). The neurocognitive bases of human
multimodal food perception: sensory integration. Neurosci. Biobehav. Rev. 30,
613–650. doi: 10.1016/j.neubiorev.2005.11.003
Zatorre, R. J., Jones-Gotman, M., and Rouby, C. (2000). Neural mechanisms
involved in odor pleasantness and intensity judgments. Neuroreport 11,
2711–2716. doi: 10.1097/00001756-200008210-00021
Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2017 Fiore and Pazzaglia. This is an open-access article distributed
under the terms of the Creative Commons Attribution License (CC BY). The
use, distribution or reproduction in other forums is permitted, provided the
original author(s) or licensor are credited and that the original publication in
this journal is cited, in accordance with accepted academic practice. No use,
distribution or reproduction is permitted which does not comply with these
terms.
Frontiers in Human Neuroscience | www.frontiersin.org 3 January 2017 | Volume 10 | Article 689


PAZZAGLIA, Mariella

Archivio della ricerca- Università di Roma La Sapienza

GENERAL COMMENTARYpublished: 09 January 2017doi: 10.3389/fnhum.2016.00689Frontiers in Human Neuroscience | www.frontiersin.org 1 January 2017 | Volume 10 | Article 689Edited by:Stephane Perrey,University of Montpellier, FranceReviewed by:Tao Zhang,Institute of Biotechnology (CAS),China*Correspondence:Mariella Pazzagliamariella.pazzaglia@uniroma1.itReceived: 19 October 2016Accepted: 26 December 2016Published: 09 January 2017Citation:Fiore A and Pazzaglia M (2017)Commentary: Cortical Plasticity andOlfactory Function in Early Blindness.Front. Hum. Neurosci. 10:689.doi: 10.3389/fnhum.2016.00689Commentary: Cortical Plasticity andOlfactory Function in Early BlindnessAlessandra Fiore 1 and Mariella Pazzaglia 1, 2*1Department of Psychology, University of Rome “La Sapienza”, Rome, Italy, 2 IRCCS Santa Lucia Foundation, Rome, ItalyKeywords: olfactory, visual, plasticity, multimodal integration, rehabilitation, motor activityA commentary onCortical Plasticity and Olfactory Function in Early Blindnessby Araneda, R., Renier, L. A., Rombaux, P., Cuevas, I., and De Volder, A. G. (2016). Front. Syst.Neurosci. 10:75. doi: 10.3389/fnsys.2016.00075Humans beings are visual creatures, which means that they preferentially map the world guidedlargely by sight (Aglioti and Pazzaglia, 2010). However, multiple senses contribute to the creationof an integrated experience of the real world (Aglioti and Pazzaglia, 2011). Among these, theolfactory sense is undoubtedly the most neglected. One of the reasons for this is that odors donot always prevail at a conscious level (Sobel et al., 1999), even though olfactory receptors arecontinuously active in order to acquire sensory, motor and affective information (Pazzaglia, 2015).A second reason is the fact that sight occasionally prevails over, or even hides, the informationprovided by other senses. In a recent stimulating and timely article, Araneda and colleaguespresented an important view of the pathophysiological mechanisms of plasticity that occur inthe visual brain of early blind patients (Araneda et al., 2016). The authors produced a behavioraland anatomo-physiological perspective on the guiding role of olfactory information when sight islacking. Behaviorally, early blind subjects perform better than sighted individuals when it comesto odor detection and awareness, indicating that the sense of smell is highly plastic and suggestingthe possibility of incremental odor processing by way of learning and experience. Neurally, activeolfactory processing occurs within the occipital cortex, suggesting the privileged access of odor toother, seemingly unrelated, sensory systems and neural regions.The study of Araneda and colleagues also provides an excellent opportunity to investigateolfactory information, not only in the complete absence of visual mediation (e.g., in congenitallyblind individuals), but also in terms of understanding the value of this extraordinary plasticityin relation to the enhanced olfactory abilities of many of our sensations, perceptions, andhigher-order cognitive processing. This is an important topic, and the contribution of cross-modalvisual-olfactory interaction can certainly be emphasized, as this is supported by much experimentalevidence in terms of highlighting the implications in the field of clinical studies. The congruentodor of an object facilities how it is visually represented (Verhagen and Engelen, 2006), andthe concurrent presence of the visual cues of a given object may also enhance olfactoryperformances (Gottfried and Dolan, 2003). The relevance of olfaction in visual areas has beendemonstrated in a causative study using repetitive transcranial magnetic stimulation, which showedthat olfactory performances improve when occipital areas in the brain are stimulated, even inseeing humans (Jadauji et al., 2012). The merging of a visual representation enables healthyindividuals to optimize their identification and discrimination of an object based on smell alone.Analogously, neuroimaging studies have reported modulation in visual cortices during purelyolfactory performances (Qureshy et al., 2000; Zatorre et al., 2000; Dade et al., 2002), hinting atgenuine cross-modal neural modulation evoked by olfactory cues. In addition to conveying visualinformation, it is known that odors also trigger more dynamic information about visual motorstates (Kuang and Zhang, 2014).Fiore and Pazzaglia Smelling Visual Objects, Actions and WorldsThe merging of visual and olfactory information facilitatesthe kinematics of reach-to-grasp movements and understandingactions (Tubaldi et al., 2011). When a person observes someoneelse grasping an object, the neurons that control the handmuscles in the observer become more alert, as if the individualis also preparing to perform the same action (Fadiga et al.,1995). If someone smells the aroma of a strawberry whilesimultaneously observing someone else grasping this fruit, theolfactory information activates in the observer the brain regionsinvolved in the congruent body movements (Rossi et al., 2008).This facilitation effect of olfaction on movement parametersis specific to the muscles that guide the observed movement(Castiello, 1997). Conversely, the perception of smelling adifferent food (orange) object did not induce any facilitation ofthe corticospinal system.Clinically, being driven by visual-olfactory inputs to themapping of actions could assuage motor disturbances. InParkinson’s disease (PD), for example (Castiello et al., 2009;Parma et al., 2013a), patients present, among other symptoms,with an impairment of the kinematics of movements. Likehealthy subjects, a clear facilitation with the kinematics ofreaching and grasping movements was found in patients withPD in conditions of coherent actions between the object andodor. This suggests that cross-modal processing optimizes, notonly perceptive, but also motor, functioning. Nevertheless, inclinical applications, the imitation of reach-to-grasp movementshas been facilitated in a condition paired with the smell ofthe subject’s own mother in Autism Spectrum Disorder (ASD)(Parma et al., 2013b). The smell of a stranger did not, however,modulate automatic visual-motor actions. Accordingly, a familiarbody odor may promote socio-cognitive behavior such as thespontaneous imitation that is impaired in ASD. Together, thesestudies show that the olfactory modality may interact withvisual-motor behavior in clinical and healthy populations inorder to integrate perceptions that, ultimately, may appear tobe exclusively visual (Pazzaglia et al., 2016). The mechanismthrough which the visual and motor system is connected tohigher-order olfactory perception is worth investigating, andcould have important clinical applications. Olfaction is probablyinteracting with vision in multiple pathways. Olfactory sourcesfor building integrated multisensory perceptions can developvery rapidly for perceiving and interacting with objects andactions. The actions triggered by the smelling source indicate thatolfactory cues may implicitly predict and trigger action planning(Pazzaglia, 2013; Pazzaglia and Galli, 2015). These interestingpossibilities await further research before this could become auseful tool in clinics. Consequently, by exploring how a greateruse of odorous stimuli contributes to visual and motor planningremains a fundamental application in a clinical perspective (Galliet al., 2015; Galli and Pazzaglia, 2015; Pazzaglia and Molinari,2016). The functional gain derived from odor integration mightoptimize rehabilitation programmes in case of generalized motorimpairment and disturbed human social interaction.AUTHOR CONTRIBUTIONSAll authors listed, have made substantial, direct and intellectualcontribution to the work, and approved it for publication.REFERENCESAglioti, S. M., and Pazzaglia, M. (2010). Representing actions through their sound.Exp. Brain Res. 206, 141–151. doi: 10.1007/s00221-010-2344-xAglioti, S.M., and Pazzaglia,M. (2011). Sounds and scents in (social) action.TrendsCogn. Sci. 15, 47–55. doi: 10.1016/j.tics.2010.12.003Araneda, R., Renier, L. A., Rombaux, P., Cuevas, I., and De Volder, A. G. (2016).Cortical Plasticity and Olfactory Function in Early Blindness. Front. Syst.Neurosci. 10:75. doi: 10.3389/fnsys.2016.00075Castiello, U. (1997). Arm and mouth coordination during the eatingaction in humans: a kinematic analysis. Exp. Brain Res. 115, 552–556.doi: 10.1007/PL00005726Castiello, U., Ansuini, C., Bulgheroni, M., Scaravilli, T., and Nicoletti, R. (2009).Visuomotor priming effects in Parkinson’s disease patients depend on thematch between the observed and the executed action. Neuropsychologia 47,835–842. doi: 10.1016/j.neuropsychologia.2008.12.016Dade, L. A., Zatorre, R. J., and Jones-Gotman, M. (2002). Olfactory learning:convergent findings from lesion and brain imaging studies in humans. Brain125, 86–101. doi: 10.1093/brain/awf003Fadiga, L., Fogassi, L., Pavesi, G., and Rizzolatti, G. (1995). Motor facilitationduring action observation: a magnetic stimulation study. J. Neurophysiol. 73,2608–2611.Galli, G., Lenggenhager, B., Scivoletto, G., Molinari, M., and Pazzaglia, M. (2015).Don’t look at my wheelchair! The plasticity of longlasting prejudice.Med. Educ.49, 1239–1247. doi: 10.1111/medu.12834Galli, G., and Pazzaglia, M. (2015). Commentary on: “The body social: an enactiveapproach to the self.” A tool for merging bodily and social self in immobileindividuals. Front. Psychol. 6:305. doi: 10.3389/fpsyg.2015.00305Gottfried, J. A., and Dolan, R. J. (2003). The nose smells what the eye sees:crossmodal visual facilitation of human olfactory perception. Neuron 39,375–386. doi: 10.1016/S0896-6273(03)00392-1Jadauji, J. B., Djordjevic, J., Lundstrom, J. N., and Pack, C. C. (2012). Modulationof olfactory perception by visual cortex stimulation. J. Neurosci. 32, 3095–3100.doi: 10.1523/JNEUROSCI.6022-11.2012Kuang, S., and Zhang, T. (2014). Smelling directions: olfaction modulatesambiguous visual motion perception. Sci. Rep. 4, 5796. doi: 10.1038/srep05796Parma, V., Bulgheroni, M., Scaravilli, T., Tirindelli, R., and Castiello, U. (2013a).Implicit olfactory processing attenuates motor disturbances in idiopathicParkinson’s disease. Cortex 49, 1241–1251. doi: 10.1016/j.cortex.2012.05.017Parma, V., Bulgheroni, M., Tirindelli, R., and Castiello, U. (2013b). Bodyodors promote automatic imitation in autism. Biol. Psychiatry 74, 220–226.doi: 10.1016/j.biopsych.2013.01.010Pazzaglia, M. (2013). Does what you hear predict what you will do and say? Behav.Brain Sci. 36, 370–371. doi: 10.1017/S0140525X12002804Pazzaglia, M. (2015). Body and odors: non just molecules, after all. Curr. Dir.Psychol. Sci. 24, 329–333. doi: 10.1177/0963721415575329Pazzaglia, M., and Galli, G. (2015). Translating novel findings of perceptual-motorcodes into the neuro-rehabilitation of movement disorders. Front. Behav.Neurosci. 9:222. doi: 10.3389/fnbeh.2015.00222Pazzaglia, M., Haggard, P., Scivoletto, G., Molinari, M., and Lenggenhager, B.(2016). Pain and somatic sensation are transiently normalized by illusory bodyownership in a patient with spinal cord injury. Restor. Neurol. Neurosci. 34,603–613. doi: 10.3233/RNN-150611Pazzaglia, M., and Molinari, M. (2016). The embodiment of assistivedevices-from wheelchair to exoskeleton. Phys. Life Rev. 16, 163–175.doi: 10.1016/j.plrev.2015.11.006Frontiers in Human Neuroscience | www.frontiersin.org 2 January 2017 | Volume 10 | Article 689Fiore and Pazzaglia Smelling Visual Objects, Actions and WorldsQureshy, A., Kawashima, R., Imran, M. B., Sugiura, M., Goto, R., Okada, K., et al.(2000). Functional mapping of human brain in olfactory processing: a PETstudy. J. Neurophysiol. 84, 1656–1666.Rossi, S., De Capua, A., Pasqualetti, P., Ulivelli, M., Fadiga, L., Falzarano, V., et al.(2008). Distinct olfactory cross-modal effects on the human motor system.PLoS ONE 3:e1702. doi: 10.1371/journal.pone.0001702Sobel, N., Prabhakaran, V., Hartley, C. A., Desmond, J. E., Glover, G. H., Sullivan,E. V., et al. (1999). Blind smell: brain activation induced by an undetectedair-borne chemical. Brain 122(Pt 2), 209–217. doi: 10.1093/brain/122.2.209Tubaldi, F., Turella, L., Pierno, A. C., Grodd, W., Tirindelli, R., and Castiello,U. (2011). Smelling odors, understanding actions. Soc. Neurosci. 6, 31–47.doi: 10.1080/17470911003691089Verhagen, J. V., and Engelen, L. (2006). The neurocognitive bases of humanmultimodal food perception: sensory integration. Neurosci. Biobehav. Rev. 30,613–650. doi: 10.1016/j.neubiorev.2005.11.003Zatorre, R. J., Jones-Gotman, M., and Rouby, C. (2000). Neural mechanismsinvolved in odor pleasantness and intensity judgments. Neuroreport 11,2711–2716. doi: 10.1097/00001756-200008210-00021Conflict of Interest Statement: The authors declare that the research wasconducted in the absence of any commercial or financial relationships that couldbe construed as a potential conflict of interest.Copyright © 2017 Fiore and Pazzaglia. This is an open-access article distributedunder the terms of the Creative Commons Attribution License (CC BY). Theuse, distribution or reproduction in other forums is permitted, provided theoriginal author(s) or licensor are credited and that the original publication inthis journal is cited, in accordance with accepted academic practice. No use,distribution or reproduction is permitted which does not comply with theseterms.Frontiers in Human Neuroscience | www.frontiersin.org 3 January 2017 | Volume 10 | Article 689