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Insights into the olfactory abilities of neurological populations. From perception to action
Full text linkAlthough smell is involved in a number of survival functions, the comprehension of olfactory processing is still far from being exhaustive.
Following a concise outline of the anatomy and the physiology underlying the olfactory system (Chapter 1), I focused on the description of the quantitative and qualitative smell distortions in patients diagnosed with olfactory disorders as to outcrop the differences between normal and pathological functioning of the sense of smell (Chapter 2). Subsequently, I moved to a higher degree of complexity by considering how odours are perceived and elaborated at a cognitive level, devoting special attention to the way people describe their own olfactory experience (Chapter 3). Chapter 4 provides a brief revision of the methodologies currently utilized to evaluate olfactory performance in humans based on the distinction between explicit (conscious-mediated) and implicit (subliminal) procedures.
The second part of the present thesis concerns the outline of the experimental work I undertook. In the first experiment (Chapter 5), I administered to a carefully selected and homogenous group of relapsing remitting multiple sclerosis patients an explicit olfactory test, the Sniffin’ Sticks Extended Test. This measure allows to evaluate specific aspects of olfactory performance, namely odour threshold, discrimination and identification as well as to ascertain participant’s general olfactory performance (TDI score). The aim of this study was twofold. First, to understand whether an explicit olfactory test can reliably display either a global or a specific olfactory loss in multiple sclerosis patients. Second, to ascertain whether alterations of some brain areas of the central nervous system can provide reliable biological markers (e.g., number and volume of white matter T2 lesions within central eminent olfactory regions) which correlate with the olfactory abnormalities in this population. On the basis of the verbalized (conscious) responses provided to the Sniffin’ Sticks Test, 34% of our multiple sclerosis sample showed a general olfactory loss compatible with hyposmia. Specifically, odour discrimination and identification (but not odour threshold) allowed to discriminate the patients with multiple sclerosis from the control group. In neural terms, no significant correlation between the number and the volume of the plaques within the central olfactory regions and the scores obtained to the behavioural test was evident. All in all, the results reported in Chapter 5 indicated that explicit olfactory testing, although very useful to screen for the presence of olfactory disturbance, might not have the potency to fully account for human olfactory processing. Further support to this contention is also given by the lack of correlation between explicit test scores and the considered biological markers.
Thus, I questioned whether explicit test procedures have the ability to uncover the presence of different forms of olfactory elaboration. Therefore, I addressed my interest to implicit olfactory testing. In order to minimize the influence of verbal abilities on odour elaboration, I capitalized on paradigms able to reveal, via the analysis of movement kinematics, how odour stimuli are processed and how they modulate motor behaviour. Chapter 6, 7 and 8 were designed in order to elucidate this issue. In Chapters 6 and 7, I investigated the effects of common odours (e.g., odours produced by inanimate sources) in two groups of patients, whose explicit olfactory abilities, as measured by means of standardized tests, were lacking. Specifically, I tested a group of functionally anosmic traumatic brain injured (Chapter 6) and idiopathic Parkinson’s disease patients (Chapter 7) to evaluate the presence of lingering implicit olfactory abilities by indirectly studying the effects odours might have on the kinematics of the moving hand. Participants were asked to perform reach-to-grasp movements towards large or small visual targets (e.g., a plastic apple or strawberry, respectively) following the delivery of olfactory cues. The odour was either ‘size’ congruent with the visual target (e.g., orange or almond, respectively), incongruent (e.g., almond or orange, respectively) or absent (e.g., fresh air).
Chapter 6 describes the outcomes of the study carried out on a group of anosmic traumatic brain injured patients. Comparing their performance to that shown by matched normosmic/microsmic traumatic brain injured patients and neurologically healthy controls it was found that all the three groups were similarly affected by the exposure to odours. In particular, interference effects were revealed. To elaborate, when participants grasped a large visual target preceded by an odour evoking a small object, a kinematic parameter indicating how hand aperture is shaped towards the visual target (i.e., maximum velocity of grip aperture) was greater than when the same visual target was grasped preceded by an odour evoking a congruent grip or when no odour was presented. This evidence seems to suggest that some sort of implicit olfactory processing is preserved in traumatic brain injured patients who fail at standardized explicit tests.
The results outlined in Chapter 7 indicate that, as neurologically healthy participants and vascular parkinsonism patients, idiopathic Parkinson’s disease patients were facilitated in the execution of their actions when exposed to an odour evoking an object that was similar in size with respect to a visual to-be-grasped target. This kind of olfactory priming resulted in an attenuation of the bradykinesia of hand transport movement and the hypometria of the grip amplitude, which are motor disturbances classically attributed to these patients. However, this facilitation effect was absent when the priming odour evoked an object different in size with respect to the visual to-be-grasped target. Altogether these results speak in favour of an adequate residual implicit olfactory elaboration in idiopathic Parkinson’s disease patients.
On the grounds of the findings from the experiments overviewed in Chapter 6 and 7, I advanced some theoretical conjectures. In order to influence behaviour, an odour processed implicitly may not require the conscious recollection of the stimulus. Therefore, implicit olfactory processing might sidestep higher cognitive function involvement and, instead, rely on the integrity of different structures. A proper candidate might be the amygdala, an area which is physically close to the olfactory brain areas and that was not compromised in the traumatic brain injured patients tested and in the early stages of Parkinson’s disease. Once confirmed, these findings could be useful when rehabilitation strategies are being hypothesized for both these populations. Indeed, the residual ability to perceive olfactory stimuli and to respond subconsciously to them could hypothetically be utilized to design trainings as to improve upper limb motor control.
In the experiments described above, patients diagnosed with olfactory loss displayed implicit olfactory processing following the exposure to common odours, as evident from the alteration of the kinematic variables of the reach-to-grasp movement. Given the differences in the neural circuits undelying the elaboration of odours characterized by different properties (e.g., a diverse degree of biological relevance), would the exposure to body odours elicit implicit odour processing in patients suffering from reduced olfactory abilities, as common odours do? The study reported in Chapter 8 was specifically tailored to answer this question.
A group of high functioning autistic children and a group of typically developing children was recruited. In order to expose them to a biologically relevant olfactory stimulus, we collected the body odours from the children’s mother axillæ. As to indirectly test implicit body odour processing, I underwent a modified version of the visuomotor priming paradigm, enriched with an olfactory cue. Classically, this paradigm reveals a motor facilitation effect induced by the pure observation of a movement on the execution of a similar action (Craighero, Fadiga, Umiltà, & Rizzolatti, 1996). Children were exposed to either their own mother’s odour, the odour of the mother of another participant or no odour. Then, they were asked to observe a model (either their mother or the mother of another participant) executing a reach-to-grasp action towards a visual target and perform the observed action, in the absence of specific instructions to imitate. As reported in Chapter 8, the analyses revealed that familiar body odours succeeded in modulating visuomotor priming effects. Although typically developing children showed visuomotor facilitation in all conditions, in high functioning autism participants such facilitation was evident only when they acted in the presence of their own mother’s odour. Taken together these results suggest that familiar body odour might have the ability to transmit some social significance to the visual target. This would lead to the proposal that implicit olfactory processing is preserved in high functioning autism participants, even though explicit olfactory testing places them within the hyposmia range. It might well be that, olfaction has the potency to help autistic people in forging social interactions.
Overall the findings of the experiments described here suggest that explicit olfactory testing might produce non-conclusive results in some neurological populations (Chapter 5) and might hide residual implicit odour processing in others (Chapters 6, 7 and 8). Moreover, the evaluation of odours’ biological relevance raise the possibility of an implicit olfactory-mediated communication.
With this in mind the advances of the present thesis are several and multifaceted. First, I applied a technique apt to investigate human sensorimotor control to the clinical domain. This methodology showed its potential to ‘catch’ facets of olfactory processing that otherwise would remain uncovered if simply considering the explicit aspects of olfactory performance (Chapter 5). It allowed to disclose residual implicit olfactory abilities in patients diagnosed with syndromes characterized by hyposmia or anosmia (Chapters 6, 7 and 8). The preservation of implicit olfactory skills in different neurological populations seems to indicate that it is a non-specific ability. The high-degree of interconnections among olfactory brain areas might provide a good explanation for the permanence of this form of olfactory elaboration in association with different patterns of brain regions malfunctioning.
Second, the present thesis extends previous literature on human olfactory processing by pointing out the existence of a dissociation between explicit and implicit olfactory processing (Chapter 6, 7 and 8), which might be reflected, in neural terms, by the involvement of different brain circuits.
Third, considering the level of biological relevance of odour stimuli in neurological populations depicts a novel aspect of the present work (Chapter 8).
Finally, on a clinical perspective, the findings reported within the present thesis (Chapter 6, 7 and 8) might be taken into account when developing new rehabilitation strategies at least for the neurological populations considered here.Sebbene gli stimoli olfattivi forniscano informazioni utili alla sopravvivenza, la comprensione dei meccanismi responsabili dell’elaborazione olfattiva è ancora lontana dall’aver prodotto conclusioni definitive.
Dopo una breve introduzione relativa alle caratteristiche anatomiche e fisiologiche del sistema olfattiva (Capitolo 1), ho focalizzato la mia attenzione sulla descrizione dei disturbi olfattivi quantitativi e qualitativi presentati da pazienti cui sono state diagnosticate alterazioni del senso dell’olfatto (Capitolo 2). Questo con lo scopo di evidenziare le differenze tra elaborazione olfattiva normale e patologica. Successivamente, ho spostato il livello di analisi ad un grado di complessità maggiore considerando il modo in cui gli odori sono percepiti ed elaborati a livello cognitivo, con particolare riferimento alle modalità con cui le persone descrivono la propria esperienza olfattiva (Capitolo 3). Il Capitolo 4 fornisce una concisa revisione delle metodologie attualmente utilizzate per valutare la prestazione olfattiva nell’uomo, distinguendole in procedure esplicite (che richiedono una mediazione consapevole) e implicite (che richiedono un’elaborazione a livello subliminale).
La seconda parte di questa tesi concerne la presentazione del lavoro sperimentale da me svolto. Nel primo esperimento (Capitolo 5) ho somministrato ad un gruppo omogeneo e altamente selezionato di pazienti con sclerosi multipla recidiva-remittente un test olfattivo esplicito, chiamato Sniffin’ Sticks Extended Test. Questa misura permette sia di valutare aspetti specifici della prestazione olfattiva, quali soglia, discriminazione e identificazione olfattiva, sia di ottenere un punteggio (TDI) che informa relativamente alla capacità olfattiva globale. Due sono gli scopi principali di questo studio. Comprendere se un test olfattivo esplicito è in grado di rilevare affidabilmente una disfunzione olfattiva globale o specifica in pazienti con sclerosi multipla. Verificare se alcune specifiche aree del sistema nervoso centrale possono fornire marcatori biologici attendibili (es., numero e volume delle placche all’interno delle principali aree olfattive centrali) che correlano con la prestazione olfattiva di questi pazienti. Sulla base di risposte verbalizzate (che raggiungono il livello di consapevolezza manifesta) al test Sniffin’ Sticks, il 34% del nostro campione di pazienti con sclerosi multipla presenta una riduzione olfattiva compatibile con l’iposmia. In particolare, le componenti di discriminazione e identificazione olfattiva (ma non quella di soglia) hanno efficacemente discriminato il gruppo di pazienti con sclerosi multipla dal gruppo di controllo. Dal punto di vista neurale, non sono state rilevate correlazioni significative tra il numero e il volume delle placche nelle regioni centrali del sistema olfattivo e i punteggi al test comportamentale. In conclusione, i risultati presentati nel Capitolo 5 indicano che l’utilizzo di test olfattivi espliciti, sebbene molto utile dal punto di vista clinico per una rapida valutazione dei disturbi olfattivi, non riesce a spiegare in modo conclusivo diversi aspetti della capacità umana di elaborare gli odori. Questa affermazione è ulteriormente supportata dalla mancata correlazione tra i punteggi al test e i marcatori biologici considerati.
Mi sono, quindi, chiesta se le procedure di valutazione esplicite potessero celare altre forme di elaborazione degli odori. Per questo ho diretto il mio interesse verso forme di valutazione olfattiva implicita. Per minimizzare l’influenza che le abilità verbali posso avere sull’elaborazione olfattiva, ho utilizzato dei paradigmi che rivelano, attraverso l’analisi della cinematica del movimento, come gli stimoli olfattivi vengono elaborati e come influenzano il comportamento motorio. Gli esperimenti inclusi nei Capitoli 6, 7 e 8 sono stati specificatamente costruiti per valutare questo aspetto. Negli esperimenti riportati nei Capitoli 6 e 7 ho studiato gli effetti di odori comuni (ovvero, prodotti da fonti inanimate) in due gruppi di pazienti che, ai test olfattivi espliciti, falliscono. In particolare, ho testato un gruppo di pazienti con esiti da trauma cranico (Capitolo 6) e con morbo di Parkinson (Capitolo 7) - considerati funzionalmente anosmici - per valutare la presenza di residue abilità olfattive implicite attraverso lo studio indiretto dell’influenza prodotta da un odore sulla cinematica dei movimenti della mano. Ai partecipanti è stato chiesto di compiere movimenti di raggiungimento-prensione verso un oggetto grande o piccolo (es., rispettivamente, una mela o una fragola di plastica) dopo aver presentano degli stimoli olfattivi. L’odore poteva richiamare (condizione congruente) o meno (condizione incongruente) la dimensione dell’oggetto da afferrare oppure poteva non essere presente (condizione di controllo). La rilevazione di effetti di facilitazione era attesa per alcune alcune variabili cinematiche quando veniva presentato un odore congruente. Ipotizzavo, invece, che la presentazione di un odore incongruente fosse legata a effetti di interferenza.
Il Capitolo 6 descrive i risultati dello studio condotto su un gruppo di pazienti anosmici con esiti di trauma cranico. Confrontando la prestazione di questi pazienti con un gruppo di pazienti con trauma cranico normosmici o lievemente microsmici e un gruppo di controlli neurologicamente sani, emerge che i tre gruppi erano influenzati in maniera analoga dalla presentazione degli stimoli olfattivi. Sebbene nei presenti gruppi non siano stati rilevati effetti di facilitazione, si evidenzia un effetto di interferenza. In particolare, quando un partecipante afferrava un oggetto grande preceduto dalla presentazione di un odore che evocava un oggetto di piccole dimensioni, uno dei parametri cinematici che indicano come la mano si conforma attorno all’oggetto (massima velocità di apertura della mano) era maggiore rispetto a quando lo stesso oggetto veniva preceduto da un odore che evocava una presa congruente alla dimensione dell’oggetto visivo o quando nessun odore veniva presentato. La presente evidenza suggerisce che una qualche forma di elaborazione olfattiva implicita permane in pazienti che falliscono ai test olfattivi espliciti.
I risultati presentati nel Capitolo 7 indicano che, analogamente ai controlli neurologicamente sani e a pazienti con parkinsonismo vascolare - che non presentano disturbi olfattivi - pazienti con diagnosi di morbo di Parkinson idiopatico erano facilitati nell’esecuzione dei azioni quando esposti a odori che evocano un oggetto di dimensioni simili a quelle dell’oggetto da afferrare. Questo tipo di preparazione basata sullo stimolo olfattivo produce una riduzione della bradicinesia del movimento di raggiungimento e dell’ipometria dell’apertura della mano, che sono identificati tra i classici disturbi motori presentati da questi pazienti. Tuttavia, tale effetto di facilitazione non si manifestava quando l’odore evocava un oggetto di dimensioni diverse rispetto a quello da afferrare. Nel complesso questi risultati sembrano supportare la presenza di un’adeguata residua elaborazione olfattiva implicita in pazienti con morbo di Parkinson idiopatico.
Sulla base dei dati prodotti dagli esperimenti riportati nei Capitoli 6 e 7, ho avanzato alcune possibili congetture teoriche. Per avere un effetto sul comportamento, l’elaborazione implicita di un odore non richiede il riconoscimento consapevole dello stimolo. Perciò, l’elaborazione olfattiva implicita sembra eludere il coinvolgimento delle funzioni cognitive superiori e sfruttare, piuttosto, l’integrità di altre aree cerebrali. Ipotizzo che l’amigdala, un’area fisicamente vicina alle aree olfattive centrali e preservata nei pazienti testati, sia un buon candidato per giocare questo ruolo. Una volta confermati, questi dati potrebbero essere utilizzati per lo sviluppo di strategie di riabilitazione per pazienti con trauma cranico e morbo di Parkinson idiopatico. Infatti, la capacità residua di percepire gli stimoli olfattivi e di rispondere inconsapevolmente in modo adeguato a tali stimoli può essere utilizzata per progettare esercizi per migliorare il controllo motorio degli arti superiori.
Negli esperimenti appena descritti, pazienti identificati come anosmici presentano preservate capacità di elaborazione implicita di odori comuni, come dimostrato dalle alterazioni cinematiche rilevate sul movimento di raggiungimento-prensione. Dato che l’elaborazione di odori caratterizzati da diverse proprietà (es., un diverso grado di rilevanza biologica) richiede l’implementazione in circuiti neurali differenti, l’esposizione a odori corporei potrebbe far emergere un’elaborazione olfattiva di carattere implicito in pazienti con ridotte abilità olfattive? Lo studio presentato nel Capitolo 8 è stato specificatamente disegnato per rispondere a questa domanda.
Un gruppo di pazienti con autismo ad alto funzionamento e un gruppo di controlli di pari età e sesso sono stati reclutati ed esposti a stimoli olfattivi biologicamente rilevanti. Gli odori sono stati raccolti da dischetti di cotone indossati sotto le ascelle dalle madri dei partecipanti. Per valutare in modo indiretto l’elaborazione implicita di questi odori, ho applicato una versione modificata del paradigma di priming visuomotorio, cui ho aggiunto una stimolazione olfattiva. Classicamente, questo paradigma rivela un effetto di facilitazione motoria indotto dalla semplice osservazione di un movimento sull’esecuzione di un’azione simile (Craighero, Fadiga, Umiltà, & Rizzolatti, 1996). I partecipanti sono stati esposti sia all’odore della loro stessa madre, all’odore della madre di un altro partecipante o a nessun odore. Successivamente, è stato chiesto loro di osservare un modello (la loro madre o la madre di un altro partecipante) mentre eseguiva un’azione di raggiungimento-prensione verso un oggetto e sono stati osservati eseguire l’azione in assenza di specifiche istruzioni relative all’imitazione del gesto. Come riportato nel Capitolo 8, le analisi rivelano che l’odore corporeo familiare è efficace nel modulare gli effetti di priming visuomotorio. Sebbene i partecipanti a sviluppo tipico presentino un effetto di facilitazione visuomotoria in tutte le condizioni, i partecipanti con autismo ad alto funzionamento presentano tale facilitazione motoria selettivamente quando esposti a
The Effect of Odour Valence and Odour Detection Threshold on the Withholding and Cancellation of Reach-to-Press Responses
Full text linkIntroduction
Withholding uninitiated actions and cancelling ongoing ones are two main components of response inhibition, a key element of the executive control. Inhibitory performance is sensitive to emotional contexts elicited by subliminal and supraliminal visual material. However, whether stimuli from other sensory modalities, such as odours, would equally modulate response inhibition remains unclear. Here, we aimed to assess the effect of task-irrelevant odours as a function of their valence and threshold on both action withholding and action cancellation of reach-to-press movements.
Method
Thirty-two healthy participants performed a Go/No-Go task that included the presentation of pleasant (orange) and unpleasant (trimethyloxazole) odour primes at supra- and sub-threshold levels; clean air was included as a control condition. The reach-to-press responses were composed of an initial release phase and a subsequent reaching phase.
Results
Only the supra-threshold pleasant (vs. control) odour impaired action withholding. Moreover, the pleasant (vs. control) odour—presented at both sub- and supra-threshold levels—elicited more accurate Go responses, whereas the sub- and supra-threshold pleasant and unpleasant (vs. control) odours triggered faster responses in the release phase. Additionally, only the supra-threshold pleasant (vs. unpleasant) odour impaired action cancellation in the reaching phase. Furthermore, reaching responses were slower following the supra-threshold unpleasant (vs. control) odour.
Conclusions
Our findings extend the sparse literature on the impact of odour stimuli on goal-directed behaviour, highlighting the role of both odour valence and threshold in the modulation of response inhibition.
Implications
Determining the mechanisms by which odour stimuli modulate response inhibition lays the foundations for research on odour-triggered disinhibition
Fetal Kinematics: Basic Outcomes and Translational Outlook
No full textThis Viewpoint examines recent developments in the quantitative characterization of fetal movements via kinematical analysis. We contend that fetal kinematics represents a powerful tool to investigate prenatal cognition and the prepostnatal continuity of cognitive development. The potential benefits of increased investigation into the kinematics of fetal movement are manifold, and apply to diverse fields including pediatric medicine and developmental biology
Sex differences in body ownership in adults with autism spectrum disorder
Full text linkA strong male prevalence has been observed in autism spectrum disorder (ASD) since its definition, but the behavioral manifestations of sex disparity have yet to be clarified. Here, we investigate sex differences in the perception of the Numbness Illusion (NI), a procedure based on a tactile conflict, in adults with ASD and with typical development. We aim to assess if women and men with ASD perceive NI-dependent body ownership differently and whether sex differences emerge in individuals with typical development. To elicit the NI, participants pressed their right-hand palm against the confederate's hand and stroked with the thumb and the index finger of their left hand the joined index fingers in a synchronous or asynchronous way. Results reveal that women with ASD present a reversed and atypical pattern for the NI compared to men with ASD and a group of matched controls. In particular, women with ASD report a stronger illusion than men with ASD, that is more evident in the asynchronous conditions. In the asynchronous condition, women in the ASD group report stronger NI as compared to women and men in the Control group, whereas men with ASD only to men in the Control group. In the typical sample, the NI emerges only in the synchronous condition and no sex difference is observed. We discuss our results in terms of potential advantage of women in sociality and sensory information processing that might lead women with ASD to use different modalities to solve the illusion compared to men with ASD. In sum, these outcomes describe sex differences in individuals with ASD in the domain of illusory perception. This may be used in the future to support the characterization of the female phenotype of autism.info:eu-repo/semantics/publishedVersio
Competitive (but not cooperative) body odors bias the discrimination of action intentions towards cooperation
Full text linkOdors help us to interpret the environment, including the nature of social interactions. But, whether and how they influence the ability to discriminate the intentional states embedded in actions is unclear. In two experiments, we asked two independent groups of participants to discriminate motor intentions from videos showing one agent performing a reach-to-grasp movement with another agent with a cooperative or a competitive intent, and the same movement performed alone at either natural- or fast-speed, as controls. Task-irrelevant odor primes preceded each video presentation. Experiment 1 (N = 19) included masked cooperative and competitive body odors (human sweat collected while the donors were engaged in cooperative and competitive activities), whereas Experiment 2 (N = 20) included a common odor (cedarwood oil) and no odor (clean air) as primes. In an odorprimed, two-alternative forced choice task, participants discriminated the intention underlying the observed action. The results indicated that the odor exposure modulated the discrimination speed across different intentions, but only when the action intentions were hard to discriminate (cooperative vs. individual natural-speed, and competitive vs. individual fast-speed). Contrary to our hypothesis, a direct odor-action intention compatibility effect was not found. Instead, we propose a negative arousal compatibility-like effect to explain our results. Discrimination of high arousing action intentions (i.e., competitive) took longer when primed by high arousing odors (common odor and competitive body odor) than by low arousing odors (cooperative body odor and no odor). Discrimination of low arousing action intentions (i.e., cooperative) took longer when primed by low arousing odors than by high arousing odors. All in all, competitive (but not cooperative) body odors bias the discrimination of action intentions towards cooperation
Visuo-olfactory integration during action observation and execution of reach to grasp movements
Full text linkObserving the actions of others prompts the motor system to perform a similar action. However, visual cues are not the only source of sensory information for the motor system, which is affected by stimuli presented in all modalities even when they are irrelevant for action completion. The current experiment explored whether (and how) olfactory stimuli can influence the performance of a reach-to-grasp movement to visual objects differing in size (small and large) in the context of an automatic imitation task. Odours could match-or not- the size of a to-be-grasped visual target, or be nonexistent. Movement duration, an integral index of motor control, was significantly shorter when participants previously observed the same action. Addition of the odour component suggested that when the odour matched the size of a small target, a facilitation effect was found. Results are discussed in terms of olfactory-visual integration mechanisms and how they relate to embodied cognition
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