An object's smell in the multisensory brain : how our senses interact during olfactory object processing

Object perception is a remarkable and fundamental cognitive ability that allows us to interpret and interact with the world we are living in. In our everyday life, we constantly perceive objects–mostly without being aware of it and through several senses at the same time. Although it might seem that object perception is accomplished without any effort, the underlying neural mechanisms are anything but simple. How we perceive objects in the world surrounding us is the result of a complex interplay of our senses. The aim of the present thesis was to explore, by means of functional magnetic resonance imaging, how our senses interact when we perceive an object’s smell in a multisensory setting where the amount of sensory stimulation increases, as well as in a unisensory setting where we perceive an object’s smell in isolation. In Study I, we sought to determine whether and how multisensory object information influences the processing of olfactory object information in the posterior piriform cortex (PPC), a region linked to olfactory object encoding. In Study II, we then expanded our search for integration effects during multisensory object perception to the whole brain because previous research has demonstrated that multisensory integration is accomplished by a network of early sensory cortices and higher-order multisensory integration sites. We specifically aimed at determining whether there exist cortical regions that process multisensory object information independent of from which senses and from how many senses the information arises. In Study III, we then sought to unveil how our senses interact during olfactory object perception in a unisensory setting. Other previous studies have shown that even in such unisensory settings, olfactory object processing is not exclusively accomplished by regions within the olfactory system but instead engages a more widespread network of brain regions, such as regions belonging to the visual system. We aimed at determining what this visual engagement represents. That is, whether areas of the brain that are principally concerned with processing visual object information also hold neural representations of olfactory object information, and if so, whether these representations are similar for smells and pictures of the same objects. In Study I we demonstrated that assisting inputs from our senses of vision and hearing increase the processing of olfactory object information in the PPC, and that the more assisting input we receive the more the processing is enhanced. As this enhancement occurred only for matching inputs, it likely reflects integration of multisensory object information. Study II provided evidence for convergence of multisensory object information in form of a non-linear response enhancement in the inferior parietal cortex: activation increased for bimodal compared to unimodal stimulation, and increased even further for trimodal compared to bimodal stimulation. As this multisensory response enhancement occurred independent of the congruency of the incoming signals, it likely reflects a process of relating the incoming sensory information streams to each other. Finally, Study III revealed that regions of the ventral visual object stream are engaged in recognition of an object’s smell and represent olfactory object information in form of distinct neural activation patterns. While the visual system encodes information about both visual and olfactory objects, it appears to keep information from the two sensory modalities separate by representing smells and pictures of objects differently. Taken together, the studies included in this thesis reveal that olfactory object perception is a multisensory process that engages a widespread network of early sensory as well higher-order cortical regions, even if we do not encounter ourselves in a multisensory setting but exclusively perceive an object’s smell

Sensor-based machine olfaction with neuromorphic models of the olfactory system

Electronic noses combine an array of cross-selective gas sensors with a pattern recognition engine to identify odors. Pattern recognition of multivariate gas sensor response is usually performed using existing statistical and chemometric techniques. An alternative solution involves developing novel algorithms inspired by information processing in the biological olfactory system. The objective of this dissertation is to develop a neuromorphic architecture for pattern recognition for a chemosensor array inspired by key signal processing mechanisms in the olfactory system. Our approach can be summarized as follows. First, a high-dimensional odor signal is generated from a chemical sensor array. Three approaches have been proposed to generate this combinatorial and high dimensional odor signal: temperature-modulation of a metal-oxide chemoresistor, a large population of optical microbead sensors, and infrared spectroscopy. The resulting high-dimensional odor signals are subject to dimensionality reduction using a self-organizing model of chemotopic convergence. This convergence transforms the initial combinatorial high-dimensional code into an organized spatial pattern (i.e., an odor image), which decouples odor identity from intensity. Two lateral inhibitory circuits subsequently process the highly overlapping odor images obtained after convergence. The first shunting lateral inhibition circuits perform gain control enabling identification of the odorant across a wide range of concentration. This shunting lateral inhibition is followed by an additive lateral inhibition circuit with center-surround connections. These circuits improve contrast between odor images leading to more sparse and orthogonal patterns than the one available at the input. The sharpened odor image is stored in a neurodynamic model of a cortex. Finally, anti-Hebbian/ Hebbian inhibitory feedback from the cortical circuits to the contrast enhancement circuits performs mixture segmentation and weaker odor/background suppression, respectively. We validate the models using experimental datasets and show our results are consistent with recent neurobiological findings

Neuronal correlates of tactile working memory in rat barrel cortex and prefrontal cortex

The neuronal mechanisms of parametric working memory \u2013 the short-term storage of graded stimuli to guide behavior \u2013 are not fully elucidated. We have designed a working memory task where rats compare two sequential vibrations, S1 and S2, delivered to their whiskers (Fassihi et al, 2014). Vibrations are a series of velocities sampled from a zero-mean normal distribution. Rats must judge which stimulus had greater velocity standard deviation, \u3c3 (e.g. \u3c31 > \u3c32 turn left, \u3c31 < \u3c32 turn right). A critical operation in this task is to hold S1 information in working memory for subsequent comparison. In an earlier work we uncovered this cognitive capacity in rats (Fassihi et al, 2014), an ability previously ascribed only to primates. Where in the brain is such a memory kept and what is the nature of its representation? To address these questions, we performed simultaneous multi-electrode recordings from barrel cortex \u2013 the entryway of whisker sensory information into neocortex \u2013 and prelimbic area of medial prefrontal cortex (mPFC) which is involved in higher order cognitive functioning in rodents. During the presentation of S1 and S2, a majority of neurons in barrel cortex encoded the ongoing stimulus by monotonically modulating their firing rate as a function of \u3c3; i.e. 42% increased and 11% decreased their firing rate for progressively larger \u3c3 values. During the 2 second delay interval between the two stimuli, neuronal populations in barrel cortex kept a graded representation of S1 in their firing rate; 30% at early delay and 15% at the end. In mPFC, neurons expressed divers coding characteristics yet more than one-fourth of them varied their discharge rate according to the ongoing stimulus. Interestingly, a similar proportion carried the stimulus signal up to early parts of delay period. A smaller but considerable proportion (10%) kept the memory until the end of delay interval. We implemented novel information theoretic measures to quantify the stimulus and decision signals in neuronal responses in different stages of the task. By these measures, a decision signal was present in barrel cortex neurons during the S2 period and during the post stimulus delay, when the animal needed to postpone its action. Medial PFC units also represented animal choice, but later in the trial in comparison to barrel cortex. Decision signals started to build up in this area after the termination of S2. We implemented a regularized linear discriminant algorithm (RDA) to decode stimulus and decision signals in the population activity of barrel cortex and mPFC neurons. The RDA outperformed individual clusters and the standard linear discriminant analysis (LDA). The stimulus and animal\u2019s decision could be extracted from population activity simply by linearly weighting the responses of neuronal clusters. The population signal was present even in epochs of trial where no single cluster was informative. We predicted that coherent oscillations between brain areas might optimize the flow of information within the networks engaged by this task. Therefore, we quantified the phase synchronization of local field potentials in barrel cortex and mPFC. The two signals were coherent at theta range during S1 and S2 and, interestingly, prior to S1. We interpret the pre-stimulus coherence as reflecting top-down preparatory and expectation mechanisms. We showed, for the first time to our knowledge, the neuronal correlates of parametric working memory in rodents. The existence of both positive and negative codes in barrel cortex, besides the representation of stimulus memory and decision signals suggests that multiple functions might be folded into single modules. The mPFC also appears to be part of parametric working memory and decision making network in rats

The Chemical Senses

Long-standing neglect of the chemical senses in the philosophy of perception is due, mostly, to their being regarded as ‘lower’ senses. Smell, taste, and chemically irritated touch are thought to produce mere bodily sensations. However, empirically informed theories of perception can show how these senses lead to perception of objective properties, and why they cannot be treated as special cases of perception modelled on vision. The senses of taste, touch, and smell also combine to create unified perceptions of flavour. The nature of these multimodal experiences and the character of our awareness of them puts pressure on the traditional idea that each episode of perception goes one or other of the five senses. Thus, the chemical senses, far from being peripheral to the concerns of the philosophy of perception, may hold important clues to the multisensory nature of perception in general

Olfactory consciousness across disciplines

Our sense of smell pervasively influences our most common behaviors and daily experience, yet little is known about olfactory consciousness. Over the past decade and a half research in both the fields of Consciousness Studies and Olfaction has blossomed, however, olfactory consciousness has received little to no attention. The olfactory systems unique anatomy, functional organization, sensory processes, and perceptual experiences offers a fecund area for exploring all aspects of consciousness, as well as a external perspective for re-examining the assumptions of contemporary theories of consciousness. It has even been suggested that the olfactory system may represent the minimal neuroanatomy that is required for conscious processing. Given the variegated nature of research on consciousness, we include original papers concerning the nature of olfactory consciousness. The scope of the special edition widely incorporates olfaction as it relates to Consciousness, Awareness, Attention, Phenomenal- or Access-Consciousness, and Qualia. Research concerning olfaction and cross-modal integration as it relates to conscious experience is also address. As the initial foray into this uncharted area of research, we include contributions from across all disciplines contributing to cognitive neuroscience, including neurobiology, neurology, psychology, philosophy, linguistics, and computer sciences. It is our hope that this Research Topic will serve as the impetus for future interdisciplinary research on olfaction and consciousness

Odorant receptor genes and their expression in migratory Atlantic salmon (Salmo salar, L.)

Being anadromous, the Atlantic salmon (Salmo salar, L.), spends part of its life cycle in fresh water and part of it at sea. They undertake return migrations of up to 4000km, negotiating complex oceanic environments, dendritic river systems and making numerous choices at river junctions to return to specific natal sites. As the fish near coastal waters, olfaction has been shown to be pivotal in the selection of the appropriate estuary and identification of the natal stream. Juvenile salmon are thought to imprint on biotic and/or abiotic environmental odours around the time of parr-smolt transformation (PST), and retain this information at least partly within the olfactory sensory neurons. These olfactory cues are then exploited with remarkable precision by adult migrants returning to the natal stream to spawn. Variation in olfactory receptors (OR) and pheromone receptors (or vomeronasal receptors: VNRs) expressed by these sensory neurons may therefore play a vital role in the maintenance of the structure of salmon populations, enabling numerous reproductively isolated communities to exist within one catchment area. Here, the isolation and characterisation of both OR and VNR genes from S.salar has facilitated further elucidation of the olfactory changes associated with parr-smolt transformation. Both sets of primary receptors have representatives expressed in male germ cells as well as olfactory tissue. Real-time quantitative RT-PCR has revealed that a group of OR genes (SORB) is expressed at a higher level during the early stages of PST. One group of VNR genes (SVRA) however, shows a peak of expression later in PST. There were also expression differences observed between families of fish. Only one family showed a significant increase in expression of SORB and SVRA, the other family presumably using other receptor types not included in this study. Molecular evidence therefore indicates that there is more than one incidence of specific-olfactory sensitivity involved in the smelting process. The stimulation of expression of two independent groups of chemosensory receptors indicates that both odours and semiochemicals play a role in olfactory imprinting. The odorant receptors involved in olfactory imprinting appear to vary between families of fish which suggests interfamilial differences in odour stimuli

Was There a Sensory Trade-off in Primate Evolution? The Vomeronasal Groove as a Means of Understanding the Vomeronasal System in the Fossil Record.

Primates have remarkable visual adaptations compared to most other mammals, long explained as associated with a trade-off with olfaction (smell). However, as more information comes to light on the role of olfaction in primate behavior it becomes apparent that olfaction is not a trivial sense. Even humans use smell to communicate, albeit in subtle ways, and the olfactory systems of the lemurs and lorises are very well-developed. Olfaction, however, is actually comprised of two distinct systems - the main olfactory and vomeronasal systems. These two systems overlap in many functions, but the main olfactory system is considered fairly generalized while the vomeronasal system is responsible for detecting odors specifically related to reproduction and predator avoidance. The vomeronasal system is incredibly variable in primates, being well-developed in the lemurs and lorises (strepsirhines) and absent in Old World monkeys and apes (catarrhines). Such variation does imply relaxed selection pressure to maintain a functional vomeronasal system in catarrhines, perhaps in response to gains in visual specialization. The goal of this dissertation is to investigate that evolutionary scenario using a multifaceted approach. A combined approach of comparing histology of the vomeronasal organ (the peripheral organ of the vomeronasal system) and computed tomography of the cranium is used to reveal variation in the vomeronasal organ across primates and to relate the soft-tissue organ to hard-tissue correlates. Indeed, the cartilage that surrounds the soft-tissue vomeronasal organ leaves a distinct impression on the nasal floor, which is here termed the vomeronasal groove . To assess the utility of inferring biological function from gross dimensions of the vomeronasal organ and its groove, vomeronasal organ length is compared to the number of genes underlying vomeronasal olfaction. To test whether or not the main olfactory system is evolving in tandem with the vomeronasal system, a hard-tissue correlate of the main olfaction (area of the cribriform plate) is compared to the number of genes encoding main olfaction. Results indicate that main olfaction and vomeronasal olfaction are affected by evolution differently and that vomeronasal organ length when adjusted for body size has a strong statistical relationship with the proportion of functional vomeronasal receptor genes across mammals. To test whether or not phylogenetic history, ecology, and reproduction strategies affect the evolution of the vomeronasal organ in primates, size-adjusted vomeronasal groove length is compared across related categories. Mating categories, probably reflecting sexual selection, appear to drive variation in vomeronasal groove length in lemurs and lorises, while color vision phenotypes appear to drive variation in the tarsiers, monkeys, and apes. The acquisition of trichromatic color vision in Old World monkeys and apes is associated with vomeronasal organ loss, but trichromatic color vision does not appear to be a primary driving force of vomeronasal organ reduction in other primates. The acquisition of high visual acuity, rather, appears to affect initial reduction in length of the vomeronasal groove in crown haplorhines. Fossils representing various stages of primate evolution show presence of the vomeronasal groove, and the presence of this groove in the recent ancestors of Old World monkeys and apes suggest that the vomeronasal organ was not lost until crown catarrhines (the group containing Old World monkeys and apes) diverged from all other primate lineages. High visual acuity, routine trichromatic color vision, environments with increased visibility, and changes in social dynamics could have shifted the way in which socio-sexual information was perceived in some primates, increasing the priority of visual and main olfactory signals over vomeronasal signals. Thus, a strict trade-off may not have occurred as much as a reallocation of sensory information from the vomeronasal system to vision and main olfaction