Characterizing functional pathways of the human olfactory system

Zhou, Guangyu; Lane, Gregory; Cooper, Stephanie J.; Kahnt, Thorsten; Zelano, Christina

doi:10.7554/elife.47177

Cited by 147 publications

(131 citation statements)

References 186 publications

(236 reference statements)

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“…First, the functional connectivity within the olfactory network, as defined by core olfactory processing regions (Seubert et al 2013), was assessed and compared between groups. Thereafter, a more specific analysis of primary olfactory cortex, defined as the regions receiving direct input from the olfactory bulb (Zhou et al 2019), was conducted, in which homotopic connectivity and regional homogeneity was compared between groups. Analyses were conducted in MATLAB 2019b.…”

Section: Functional Connectivity Analysesmentioning

confidence: 99%

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

Peter

Fransson

Mårtensson

et al. 2020

Preprint

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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.

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Section: Functional Connectivity Analysesmentioning

confidence: 99%

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

Peter

Fransson

Mårtensson

et al. 2020

Preprint

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“…Therefore, the sensory consequences of an odor are integrated with the ongoing high-order cognitive activity. From a neural view point, the olfactory networks still remain largely unexplored despite strong evidence of their involvement in the activation of a network of brain areas typically responsible for high-order processes (Zhou et al 2019). Similarly, the auditory system presents characteristics that predominate other senses (Aglioti & Pazzaglia 2010), with sounds helping to establish a state of alertness, predict upcoming events, and trigger anticipatory representations (Aglioti & Pazzaglia 2011).…”

Section: Introductionmentioning

confidence: 99%

Above and beyond the concrete: The diverse representational substrates of the predictive brain

Gilead¹,

Trope²,

Liberman³

2019

Behav Brain Sci

125

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Abstract In recent years, scientists have increasingly taken to investigate the predictive nature of cognition. We argue that prediction relies on abstraction, and thus theories of predictive cognition need an explicit theory of abstract representation. We propose such a theory of the abstract representational capacities that allow humans to transcend the “here-and-now.” Consistent with the predictive cognition literature, we suggest that the representational substrates of the mind are built as a hierarchy, ranging from the concrete to the abstract; however, we argue that there are qualitative differences between elements along this hierarchy, generating meaningful, often unacknowledged, diversity. Echoing views from philosophy, we suggest that the representational hierarchy can be parsed into: modality-specific representations, instantiated on perceptual similarity; multimodal representations, instantiated primarily on the discovery of spatiotemporal contiguity; and categorical representations, instantiated primarily on social interaction. These elements serve as the building blocks of complex structures discussed in cognitive psychology (e.g., episodes, scripts) and are the inputs for mental representations that behave like functions, typically discussed in linguistics (i.e., predicators). We support our argument for representational diversity by explaining how the elements in our ontology are all required to account for humans’ predictive cognition (e.g., in subserving logic-based prediction; in optimizing the trade-off between accurate and detailed predictions) and by examining how the neuroscientific evidence coheres with our account. In doing so, we provide a testable model of the neural bases of conceptual cognition and highlight several important implications to research on self-projection, reinforcement learning, and predictive-processing models of psychopathology.

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“…Due to signal susceptibility at the tissue-air conjunction, we observed considerable signal dropout in the left hemisphere at the bottom of the frontal lobe and the fronto-temporal junction, affecting key regions of interest (in the posterior OFC and APC). In light of predominantly ipsilateral olfactory pathways (Shipley and Ennis, 1996) and similar functional connectivity between the hemispheres (Zhou et al, 2019), we confined our olfactory network analysis to the right hemisphere where fMRI signals at the susceptible areas were well preserved. Table 1 shows centroid coordinates, sizes, and mean correlation coefficients (among the ROIs and among the whole brain) for all ROIs.…”

Section: Regions Of Interestmentioning

confidence: 99%

“…The largely subcortical composition of the olfactory system, with many loci at the air-tissue interface, has presented a serious challenge to olfactory network identification, especially for unguided, whole-brain rs-fMRI connectivity analysis. However, important insights into the olfactory network have been gained by targeting olfactory regions of interest (ROIs) (Plailly et al, 2008;Krusemark and Li, 2012;Krusemark et al, 2013;Sunwoo et al, 2015;Kollndorfer et al, 2015;Novak et al, 2015;Karunanayaka et al, 2017;Milardi et al, 2017;Fjaeldstad et al, 2017;Cecchetto et al, 2019), especially in combination with network-science analysis (Meunier et al, 2014;Royet et al, 2011;Ripp et al, 2018;Zhou et al, 2019). The olfactory ROIs are fairly reliably identified, but inconsistencies in network composition and connections also abound in this literature (Fjaeldstad et al, 2017;Cecchetto et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Functional connectome analyses reveal a highly optimized human olfactory network

Arnold

You

Ding

et al. 2019

Preprint

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The olfactory system is uniquely heterogeneous, performing multifaceted functions (beyond basic sensory processing) across diverse, widely distributed neural substrates. While knowledge of human olfaction continues to grow, it remains unclear how the olfactory network is organized to serve this unique set of functions. Leveraging a large and high-quality resting-state functional magnetic resonance imaging (rs-fMRI) dataset of nearly 900 participants from the Human Connectome Project (HCP), we identified a human olfactory network encompassing cortical and subcortical regions across the temporal and frontal lobes. Highlighting its reliability and generalizability, the connectivity matrix of this olfactory network mapped closely onto that extracted from an independent rs-fMRI dataset. Graph theoretical analysis further explicated the organizational principles of the network. The olfactory network exhibits a functionally advantageous modular composition of three (i.e., the sensory, limbic, and frontal) subnetworks and demonstrates strong small-world properties, high in both global integration and local segregation (i.e., circuit specialization). This network organization thus ensures the segregation of local circuits, which are nonetheless integrated via connecting hubs (i.e., amygdala and anterior insula), thereby enabling the specialized, yet integrative, functions of olfaction. In particular, the degree of local segregation positively predicted olfactory discrimination performance in the independent sample. In sum, an olfactory functional network has been identified through the large HCP dataset, affording a representative template of the human olfactory functional neuroanatomy. Importantly, the topological analysis of the olfactory network provides network-level insights into the remarkable functional specialization and spatial segregation of the olfactory system. Significance StatementOlfaction is an intriguing multifunctional system, playing key roles in regulating emotions, autonomic tone, and feeding, beyond basic sensory perception. However, it is unclear how the neuroanatomy of olfaction is organized in humans to subserve these functions. Functional connectivity analysis of the HCP dataset combined with graph theoretical analysis revealed an optimized large-scale network consisting of three subnetworks-the sensory, limbic, and frontal subnetworks. Distributed across frontal and temporal lobes in well segregated fashion, these olfactory structures are also highly integrated, linked through hub nodes of the amygdala and anterior insula. Our independent dataset replicated the HCP-derived olfactory network and, importantly, highlighted a direct association between the degree of network segregation and olfactory perception.

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Characterizing functional pathways of the human olfactory system

Cited by 147 publications

References 186 publications

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

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

Above and beyond the concrete: The diverse representational substrates of the predictive brain

Functional connectome analyses reveal a highly optimized human olfactory network

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