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Peter, M. G.

Publications and source records attributed to Peter, M. G..

7 recordsLinked to original sources

Auditory and visual object processing in olfactory cortex of individuals with life-long olfactory deprivation

The traditional view of modality-specific brain organization has been challenged by demonstrations of cross-modal processing, i.e. the activation of sensory cortex by atypical sensory input. An alternative theory suggests that rather than specializing simply in different sensory modalities, different parts of the cortex can specialize in different types of tasks. We recently addressed this question in the olfactory domain, showing that in normosmic individuals, the primary olfactory cortex (piriform cortex) responds to unimodal auditory and visual objects, regardless of how strongly they are associated with an odor. Here, we assess whether previous olfactory experience is a prerequisite for this cross-modal processing in the piriform cortex, using a unique group of individuals born without a sense of smell (congenital anosmia; CA; n = 30). First, we were able to confirm the presence of clear visual and auditory activations in the piriform cortex of these sensory deprived individuals. As compared to normosmic controls (n = 30), these activations and associated functional connectivity, both within the piriform cortices and between piriform cortex and other regions, were altered in a modality dependent way. Our results show that life-long absence of olfactory input does not impede cross-modal activations by visual and auditory objects in the piriform cortex and are compatible with the idea of a task-based rather than modality-specific organization of this brain region.

neuroscience↗

Whither unisensory olfactory cortex: processing of visual and auditory stimuli in olfactory cortex, independently of odor associations

Primary sensory cortices have been demonstrated to process sensory input from non-preferred sensory modalities, e.g. primary visual cortex reacting to auditory stimulation, bringing their presumed sensory specificity into question. Whether this reflects processing of the non-preferred stimulus per se or originates from cross-modal associations is debated. Visual/auditory objects typically have strong reciprocal associations; hence, it is difficult to address this question in these modalities. Here, we attempt to dissociate between the two competing hypotheses of whether this form of activation in primary cortices is caused by unisensory processing or cross-modal associations by turning to the olfactory system where cross-modal associations are generally weaker. Using unisensory visual and auditory objects with odor associations ranging from none to strong, we show that the posterior piriform cortex, an area known to process odor objects, is activated by both sounds and pictures of objects. Critically, this activation is independent of the objects odor associations, thereby demonstrating that the activity is not due to cross-modal associations. Using a Floyd-Warshall algorithm, we further show that the amygdala mediate condition-relevant information between the posterior piriform cortex and both the auditory and visual object-oriented cortices. Importantly, we replicate past findings of clear crossmodal processing in the visual and auditory systems. Our study demonstrates processing of non-olfactory input in olfactory cortices that is independent of cross-modal associations and contributes to a more nuanced view of modality specificity in olfactory, auditory, and visual cortices.

neuroscience↗

Lifelong olfactory deprivation-dependent cortical reorganization restricted to orbitofrontal cortex

Prolonged sensory deprivation has repeatedly been linked to cortical reorganization. We recently demonstrated that individuals with congenital anosmia (CA, complete olfactory deprivation since birth) have seemingly normal morphology in piriform (olfactory) cortex despite profound morphological deviations in the orbitofrontal cortex (OFC), a finding contradictory to both the known effects of blindness on visual cortex and to the sparse literature on brain morphology in anosmia. To establish whether these unexpected findings reflect the true brain morphology in CA, we first performed a direct replication of our previous study. Individuals with CA (n=30) were compared to age and sex matched controls (n=30) using voxel- and surface-based morphometry. The replication results were near identical to the original study: bilateral clusters of group differences in the OFC, including CA atrophy around the olfactory sulci and volume increases in the medial orbital gyri. Importantly, no group differences in piriform cortex were detected. Subsequently, to assess any subtle patterns of group differences not detectable by our mass-univariate analysis, we explored the data from a multivariate perspective. Combining the newly collected data with data from the replicated study (CA=49, Control=49) we performed support vector machine classification based on gray matter volume. In line with the mass-univariate analyses, the multivariate analysis could accurately differentiate between the groups in bilateral OFC (75-96% accuracy), whereas the classification accuracy in piriform cortex was at chance level. Our results suggest that despite lifelong olfactory deprivation, piriform (olfactory) cortex is morphologically unaltered and the morphological deviations in CA are confined to the OFC.

neuroscience↗

Acquired olfactory loss alters functional connectivity and morphology

Removing function from a developed and functional sensory system is known to alter both cerebral morphology and functional connections. To date, a majority of studies assessing sensory-dependent plasticity have focused on effects from either early onset or long-term sensory loss and little is known how the recent sensory loss affects the human brain. With the aim of determining how recent sensory loss affects cerebral morphology and functional connectivity, we assessed differences between individuals with acquired olfactory loss (duration 7-36 months, n=20) and matched healthy controls (n=23) in their grey matter volume, using multivariate pattern analyses, and functional connectivity, using dynamic connectivity analyses, within and from the olfactory cortex. Our results demonstrate that acquired olfactory loss alters grey matter volume in, among others, posterior piriform cortex, a core olfactory processing area, as well as the inferior frontal gyrus and angular gyrus. In addition, compared to controls, individuals with acquired anosmia displayed significantly stronger dynamic functional connectivity from the posterior piriform cortex to, among others, the angular gyrus, a known multisensory integration area. No significantly stronger connectivity in healthy control participants were demonstrated. When assessing differences in dynamic functional connectivity from the angular gyrus, individuals with acquired anosmia had stronger connectivity from the angular gyrus to areas primary responsible for basic visual and taste processing. These results demonstrate that recently acquired sensory loss alters both cerebral morphology within core olfactory areas and increase dynamic functional connectivity from olfactory cortex to cerebral areas processing multisensory integration.

neuroscience↗

Normal Olfactory Functional Connectivity Despite Life-Long Absence of Olfactory Experiences

Congenital blindness is associated with atypical morphology, and functional connectivity within and from, visual cortical regions; changes that are hypothesized to originate from a life-long absence of visual input and could be regarded as a general (re)organization principle of sensory cortices. Challenging this is the fact that individuals with congenital anosmia (life-long olfactory sensory loss) display little to no morphological changes in primary olfactory cortex. To determine whether olfactory input from birth is essential to establish and maintain normal functional connectivity in olfactory processing regions, akin to the visual system, we assessed differences in functional connectivity within olfactory cortex between individuals with congenital anosmia (n=33) and matched controls (n=34). Specifically, we assessed differences in connectivity between core olfactory processing regions as well as differences in regional homogeneity and homotopic connectivity within primary olfactory cortex. In contrast to congenital blindness, none of the analyses indicated atypical connectivity in individuals with congenital anosmia. In fact, post-hoc Bayesian analysis provided support for an absence of group differences. These results suggest that a lifelong absence of olfactory experience has limited impact on the functional connectivity in olfactory cortex, a finding that indicates a clear difference between sensory modalities in how sensory cortical regions develop.

neuroscience↗

Divergent morphological changes within the orbitofrontal cortex in individuals with congenital olfactory sensory loss

Individuals with congenital sensory loss usually demonstrate altered brain morphology in areas associated with early processing of the lost sense. Here, we aimed to establish whether this also applies to individuals born without a sense of smell (congenital anosmia) by comparing cortical morphology between 33 individuals with isolated congenital anosmia and matched controls. We detected no structural alterations in the primary olfactory (piriform) cortex. However, individuals with anosmia demonstrated gray matter volume atrophy in bilateral olfactory sulci, explained by decreased cortical area, curvature, and sulcus depth. They further demonstrated increased gray matter volume and cortical thickness in the medial orbital gyri; regions closely associated with olfactory processing, sensory integration, and value-coding. Our results suggest that a lifelong absence of sensory input does not necessarily lead to morphological alterations in primary sensory cortex and extend previous findings with divergent morphological alterations in bilateral orbitofrontal cortex, indicating influences of different plastic processes.

neuroscience↗

Sensory Loss Enhances Multisensory Integration Performance

Auditory and visual sensory loss has repeatedly been shown to alter abilities in remaining sensory modalities. It is, however, unclear whether sensory loss also impacts multisensory integration; an ability that is fundamental for the perception of the world around us. We determined effects of olfactory sensory deprivation on multisensory perception by assessing temporal as well as semantic aspects of audio-visual integration in 37 individuals with anosmia (complete olfactory sensory loss) and 37 healthy, matched controls. Participants performed a simultaneity judgement task to determine the temporal binding window, and a multisensory object identification task with individually degraded, dynamic visual, auditory, and audio-visual stimuli. Individuals with anosmia demonstrated an increased ability to detect multisensory temporal asynchronies, represented by a narrowing of the audio-visual temporal binding window. Furthermore, individuals with congenital, but not acquired, anosmia demonstrated indications of greater benefits from bimodal, as compared to unimodal, stimulus presentation when faced with degraded, semantic information. This suggests that the absence of the olfactory sense alters multisensory integration of remaining senses by sharpening the perception of cross-modal temporal violations, independent of sensory loss etiology. In addition, congenital sensory loss may further lead to increased gain from multisensory, compared to unisensory, information. Taken together, multisensory compensatory mechanisms at different levels of perceptual complexity are present in individuals with anosmia.

neuroscience↗