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Lundstrom, J. N.

Publications and source records attributed to Lundstrom, J. N..

14 recordsLinked to original sources

Precision measurement of non-conscious avoidance reactions using 3D tracking: Validation across olfaction and vision

One of our sensory systems key functions is to detect threats in the environment. Sensory information eliciting negative emotions, such as fear or disgust, triggers instinctive avoidance reactions. This core survival mechanism is believed to be expressed as subtle non-conscious postural reactions, even when participants are instructed to stand still. Such avoidance behavior has mainly been studied using indirect measures that make participants aware of their posture (e.g. force-plate based methods) or measures that depend on explicit cognitive tasks, like moving a joystick to indicate an urge to approach or avoid the stimulus; experimental tasks with limited ecological validity and generalizability. Therefore, despite the importance of this basic survival strategy, its underlying mechanisms are still poorly understood. Here, we used a novel 3D-camera-based method allowing direct but implicit measures of postural reactions with high precision. Participants are aware that they are being filmed but, crucially, are not informed that distance measures are obtained. We assessed this ecologically valid measure of approach/avoidance responses in two different sensory modalities: olfaction and vision. Participants were standing upright while exposed to either olfactory or visual stimuli and verbally rating their perceived valence in each trial. In response to subjectively unpleasant odors and images, participants moved away from the stimulus source, as compared to pleasant stimuli. These results demonstrate a putative modality-independent early proxy for avoidance behavior in response to perceived negative valence. Considering its face validity and general applicability, this novel experimental method presents new possibilities for assessing non-conscious approach-avoidance responses in humans.

neuroscience↗

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↗

Limited Effects of Isolated Congenital Anosmia on Cerebral White Matter Morphology

Lack of sensory input is associated with alterations in brain morphology; mainly in or near cerebral regions normally devoted to processing of the missing sense. We have in multiple studies demonstrated that the only consistent morphological finding within the gray matter of individuals born without the sense of smell (isolated congenital anosmia; ICA), are changes in or near the olfactory sulcus. For the connecting tissue of the brain, the white matter (WM), previous studies have yielded inconsistent findings. Here, we show that individuals with ICA (n=49) exhibit alterations in WM volume as compared to age- and sex-matched controls. Consistent evidence from both voxel-based morphometry and multi-voxel pattern analysis shows that individuals with ICA show decreased WM in areas surrounding the olfactory sulcus. Importantly, no WM alterations were found in areas surrounding the olfactory (piriform) cortex. In contrast to congenital sensory loss in other systems, we show that morphological alterations due to lifelong olfactory deprivation are limited. Alterations are primarily localized around the olfactory sulcus and likely due to the absence of olfactory bulbs. A possible explanation for the lack of major morphological alterations in individuals with congenital anosmia is that the olfactory regions may be recruited for non-olfactory functions.

neuroscience↗

Olfactory bulb and cortex activity reflects subjective odor intensity perception rather than concentration

Understanding stimulus intensity processing is fundamental in sensory science, yet this question remains largely unexplored in human olfaction. We investigated how the human olfactory bulb (OB) and piriform cortex (PC) process odor concentration versus subjective perceived intensity. We demonstrate that OB-PC network oscillatory dynamics are predominantly driven by perceived intensity, not physical concentration. The OB initially processes and communicates perceived intensity to the PC via early gamma-band oscillations (bottom-up feedback). The PC then refines and sends this percept back to the OB via later beta-band oscillations (top-down feedback), updating the OBs gamma activity for subsequent odorants. Critically, analyses of phase-amplitude coupling and beta burst activity demonstrate that transient beta patterns from the PC update OB gamma activity, providing the OB with an updated internal representation of the odor percept. These results reveal an oscillatory mechanism by which the olfactory system maintains perceptual constancy and adaptability despite fluctuations in environmental odor concentrations.

neuroscience↗

The Respiratory-Pupillary Phase Effect: Pupils size is smallest around inhalation onset and largest during exhalation

The prevailing view in the study of animal and human pupillary function has been that pupils dilate and are largest during inhalation and constrict and are smallest during exhalation. However, this notion has recently been challenged. Here, we systematically address this question by conducting a study encompassing three experiments (two resting tasks and one visual perception task), with the latter two being pre-registered. Collectively, across nasal and oral breathing, resting, and task conditions, our experiments consistently and robustly demonstrate that pupil size is smallest around inhalation onset and largest around peak exhalation. This phenomenon, which we term the Respiratory-Pupillary Phase Effect (RPPE), directly contradicts the long-held notion that pupils are largest during inhalation and smallest during exhalation. Notably, the dilation and constriction processes overlap with both phases. The observed consistency and significance of the RPPE across various conditions underscore the need for further investigation into its underlying mechanisms and potential impact on human behavior.

physiology↗

Distinct Functions for Beta and Alpha Bursts in Gating of Human Working Memory

Multiple neural mechanisms underlying gating to and from working memory (WM) have been proposed, with divergent results obtained in human and animal studies. Previous results from non-human primate studies suggest information encoding and retrieval is regulated by high-power bursts in the beta frequency range, whereas human studies suggest that alpha power in sensory regions filters out unwanted stimuli from entering WM. Discrepancies between studies, whether due to differences in analysis, species, or cortical regions, remain unexplained. We addressed this by performing similar single-trial burst analysis we earlier deployed on non-human primates on human whole-brain electrophysiological activity. Participants performed a sequential working memory task that allowed us to track the distinct electrophysiological activity patterns associated with neural processing of targets and distractors. Intriguingly, our results reconcile earlier findings by demonstrating that both alpha and beta bursts are involved in the filtering and control of WM items, but with region and task-specific differences between the two rhythms. Occipital beta burst patterns regulate the transition from sensory processing to WM retention whereas prefrontal and parietal beta bursts track sequence order and proactively suppress retained information prior to upcoming target encoding. Occipital alpha bursts instead suppress unwanted sensory stimuli during their presentation. These results suggest that human working memory is regulated by multiple neural mechanisms that operate in different cortical regions and serve distinct computational roles.

neuroscience↗

Metabolic state modulates neural processing of odors in the human olfactory bulb

The olfactory and endocrine systems have recently been shown to reciprocally shape the homeostatic processes of energy intake. As demonstrated in animal models, the individuals metabolic state dynamically modulates how the olfactory bulb process odor stimuli using a range of endocrine signals. Here we aimed to determine whether the neural processing of odors in human olfactory bulb is modulated by metabolic state. Participants were exposed to food-associated odors, in separate sessions being hungry and sated, while neural responses from the olfactory bulb was obtained using electrobulbogram. We found significantly higher gamma power activity (51-100Hz) in the OBs response to odors during the Hunger compared to Sated condition. Specifically, EBG gamma power were elevated while hungry already at 100ms after odor onset, thereby suggesting intra-bulbar modulation according to metabolic state. These results demonstrate that, akin to other animal models, hunger state affects OB activity in humans. Moreover, we show that the EBG method has the potential to measure internal metabolic states and, as such, could be used to study specificities in olfactory processing of individuals suffering from pathologies such as obesity or anorexia.

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↗

ODOR IDENTITY CAN BE EXTRACTED FROM THE RECIPROCAL CONNECTIVITY BETWEEN OLFACTORY BULB AND PIRIFORM CORTEX IN HUMANS

Neuronal oscillations route external and internal information across brain regions. In the olfactory system, the two central nodes--the olfactory bulb (OB) and the piriform cortex (PC)--communicate with each other via neural oscillations to shape the olfactory percept. Communication between these nodes have been well characterized in non-human animals but less is known about their role in the human olfactory system. Using a recently developed and validated EEG-based method to extract signals from the OB and PC sources, we show in healthy human participants that there is a bottom-up information flow from the OB to the PC in the beta and gamma frequency bands, while top-down information from the PC to the OB is facilitated by delta and theta oscillations. Importantly, we demonstrate that there was enough information to decipher odor identity above chance from the low gamma in the OB-PC oscillatory circuit as early as 100ms after odor onset. These data further our understanding of the critical role of bidirectional information flow in human sensory systems to produce perception. However, future studies are needed to determine what specific odor information is extracted and communicated in the information exchange.

neuroscience↗

The perception of odor pleasantness is shared across cultures

Human sensory experience varies across the globe. Nonetheless, all humans share sensory systems with a common anatomical blueprint. In olfaction, it is unknown to what degree sensory perception, in particular the perception of odor pleasantness, is dictated by universal biological principles versus sculpted by culture. To address this issue, we asked 235 individuals from 9 diverse non-western cultures to rank the hedonic value of monomolecular odorants. We observed substantial global consistency, with molecular identity explaining 41% of the variance in individual pleasantness rankings, while culture explained only 6%. These rankings were predicted by the physicochemical properties of out-of-sample molecules and out-of-sample pleasantness ratings given by a separate group of industrialized western urbanites, indicating human olfactory perception is strongly constrained by universal principles.

animal behavior and cognition↗

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↗

Adverse caregiving in infancy blunts neural processing of the mother: Translating across species

The roots of psychopathology frequently take shape during infancy in the context of parent-infant interactions and adversity. Yet, neurobiological mechanisms linking these processes during infancy remain elusive. Here, using responses to attachment figures among infants who experienced adversity as a benchmark, we assessed rat pup cortical Local Field Potentials (LFP) and behaviors exposed to adversity in response to maternal rough and nurturing handling by examining its impact on pup separation-reunion with the mother. We show that during adversity, pup cortical LFP dynamic range decreased during nurturing maternal behaviors, but was minimally impacted by rough handling. During reunion, adversity-experiencing pups showed aberrant interactions with mother and blunted cortical LFP. Blocking pup stress hormone during either adversity or reunion restored typical behavior, LFP power, and cross-frequency coupling. This translational approach suggests adversity-rearing produces a stress-induced aberrant neurobehavioral processing of the mother, which can be used as an early biomarker of later-life pathology.

neuroscience↗

Non-invasive recording from the human olfactory bulb

Current methods can, in a non-invasive manner, assess neural activity in all areas of the human brain but the olfactory bulb (OB). The OB is intimately involved in a long list of olfactory tasks, has been suggested to fulfill a role comparable to that of V1 and the thalamus in the visual system, and have been closely linked to a wide range of neuropathologies. Here we present a method for non-invasive recording of signals from the human OB with millisecond precision. We demonstrate that signals obtained via recordings from EEG electrodes at the nasal bridge represent responses from the olfactory bulb - recordings we term Electrobulbogram (EBG). The EBG is localized to the OB, is reliable, and follows response patterns demonstrated in non-human animal models. The EBG will aid future olfactory-related translational work but can also easily be implemented as an everyday clinical tool to detect pathology-related changes in human central olfactory processing in neurodegenerative diseases.

neuroscience↗