The Emergence of Synaesthesia in a Neuronal Network Model via Changes in Perceptual Sensitivity and Plasticity

Synaesthesia is an unusual perceptual experience in which an inducer stimulus triggers a percept in a different domain in addition to its own. To explore the conditions under which synaesthesia evolves, we studied a neuronal network model that represents two recurrently connected neural systems. The interactions in the network evolve according to learning rules that optimize sensory sensitivity. We demonstrate several scenarios, such as sensory deprivation or heightened plasticity, under which synaesthesia can evolve even though the inputs to the two systems are statistically independent and the initial cross-talk interactions are zero. Sensory deprivation is the known causal mechanism for acquired synaesthesia and increased plasticity is implicated in developmental synaesthesia. The model unifies different causes of synaesthesia within a single theoretical framework and repositions synaesthesia not as some quirk of aberrant connectivity, but rather as a functional brain state that can emerge as a consequence of optimising sensory information processing.     

Contributions of electric fish to the understanding of sensory processing by reafferent systems.

Sensory systems must solve the inverse problem of determining environmental events based on patterns of neural activity in the central nervous system that are affected by those environmental events. Different environmental events can give rise to indistinguishable patterns of neural activity, so that there will often, perhaps even always, be multiple solutions to a sensory inverse problem. Imaging strategies and brain organization confine these multiple solutions within a bounded set. Three different active strategies may be employed by animals to constrain the number of solutions to the sensory inverse problem: active generation of the energy (carrier) that stimulates receptors; reorientation of the point of view; and control of signal conditioning before transduction (pre-receptor mechanisms). This paper describes how these strategies are used in sensory-motor systems, using electric fish as a paradigmatic example. Carrier generation and receptor tuning to the carrier improve signal to noise ratio. Receptor tuning to different frequency bands of the carrier spectrum allows a sensory system to evaluate different kinds of carrier modulations and to extract the different features of objects in the environment. Pre-receptor mechanisms condition the signals, optimizing their detection at a foveal region where the sensory resolution is maximum. Active orientation of the sensory surface redirects the fovea to explore in detail the source of interesting signals. Sensory input generated by these active exploration mechanisms ('reafference') has two components: one, necessary, derived from the self-generated actions and another, contingent, consisting of the information obtained from the external world. Extracting environmental information ('exafference') requires that the self generated afference be subtracted from the sensory inflow. Such subtraction is often associated with the generation and storage of expectations about sensory inputs. It can be concluded that an animal's perceptual world and its ability to transform the world are inextricably linked. Understanding sensory systems must, therefore, always require understanding the organization of motor behavior.     

How do features of sensory representations develop?

Sensory representations in the brainstem and cortex have a number of features that support the idea that neural activity patterns are important in their development. Many of these features vary across species in ways that could result from perturbances in the balance of the effects of activity patterns and position-dependent gene expression. (1) Most notably, disruptions or septa in sensory maps often reflect actual discontinuities in the receptor sheet, and the discontinuities may be reflected in a series of interconnected maps. Species with different disruption patterns in sensory sheets have different matching disruption patterns in the sensory maps and variant individuals and strains of the same species have matching variations in the receptor disruption patterns and their sensory maps. (2) In addition, mutations that misdirect some of the retinal afferents from one side of the brain to the other create new sensory maps that preserve continuities in the altered pattern of input, while creating new structural discontinuities. (3) Furthermore, functionally different classes of afferents that are mixed in the receptor sheet often segregate to activate separate populations of target cells. (4) Finally, early developing portions of receptor sheets may gain more than their share of territory in sensory maps. These and other variable features of sensory maps are most readily accommodated by theories that involve roles for instruction by evoked and spontaneous neural activity patterns.     

Coevolution of visual signals and eye morphology in Polistes paper wasps

To be effective, signals must propagate through the environment and be detected by receivers. As a result, signal form evolves in response to both the constraints imposed by the transmission environment and receiver perceptual abilities. Little work has examined the extent to which signals may act as selective forces on receiver sensory systems to improve the efficacy of communication. If receivers benefit from accurate signal assessment, selection could favour sensory organs that improve discrimination of established signals. Here, we provide evidence that visual resolution coevolves with visual signals in Polistes wasps. Multiple Polistes species have variable facial patterns that function as social signals, whereas other species lack visual signals. Analysis of 19 Polistes species shows that maximum eye facet size is positively associated with both eye size and presence of visual signals. Relatively larger facets within the eye''s acute zone improve resolution of small images, such as wasp facial signals. Therefore, sensory systems may evolve to optimize signal assessment. Sensory adaptations to facilitate signal detection may represent an overlooked area of the evolution of animal communication.     

Synergism,Bifunctionality, and the Evolution of a Gradual Sensory Trade-off in Hummingbird Taste Receptors

Sensory receptor evolution can imply trade-offs between ligands, but the extent to which such trade-offs occur and the underlying processes shaping their evolution is not well understood. For example, hummingbirds have repurposed their ancestral savory receptor (T1R1–T1R3) to detect sugars, but the impact of this sensory shift on amino acid perception is unclear. Here, we use functional and behavioral approaches to show that the hummingbird T1R1–T1R3 acts as a bifunctional receptor responsive to both sugars and amino acids. Our comparative analyses reveal substantial functional diversity across the hummingbird radiation and suggest an evolutionary timeline for T1R1–T1R3 retuning. Finally, we identify a novel form of synergism between sugars and amino acids in vertebrate taste receptors. This work uncovers an unexplored axis of sensory diversity, suggesting new ways in which nectar chemistry and pollinator preferences can coevolve.     

Consciousness without cortex

Sensory consciousness — the awareness and ability to report subjective experiences — is a property of biological nervous systems that has evolved out of unconscious processing over hundreds of millions of years. From which brain structures and based on which mechanisms can conscious experience emerge? Based on the body of work in human and nonhuman primates, the emergence of consciousness is intimately associated with the workings of the mammalian cerebral cortex with its specific cell types and layered structure. However, recent neurophysiological recordings demonstrate a neuronal correlate of consciousness in the pallial endbrain of crows. These telencephalic integration centers in birds originate embryonically from other pallial territories, lack a layered architecture characteristic for the cerebral cortex, and exhibit independently evolved pallial cell types. This argues that the mammalian cerebral cortex is not a prerequisite for consciousness to emerge in all vertebrates. Rather, it seems that the anatomical and physiological principles of the telencephalic pallium offer this structure as a brain substrate for consciousness to evolve independently across vertebrate phylogeny.     

Comparing Apples and Oranges: Fold-Change Detection of Multiple Simultaneous Inputs

Sensory systems often detect multiple types of inputs. For example, a receptor in a cell-signaling system often binds multiple kinds of ligands, and sensory neurons can respond to different types of stimuli. How do sensory systems compare these different kinds of signals? Here, we consider this question in a class of sensory systems – including bacterial chemotaxis- which have a property known as fold-change detection: their output dynamics, including amplitude and response time, depends only on the relative changes in signal, rather than absolute changes, over a range of several decades of signal. We analyze how fold-change detection systems respond to multiple signals, using mathematical models. Suppose that a step of fold F₁ is made in input 1, together with a step of F₂ in input 2. What total response does the system provide? We show that when both input signals impact the same receptor with equal number of binding sites, the integrated response is multiplicative: the response dynamics depend only on the product of the two fold changes, F₁F₂. When the inputs bind the same receptor with different number of sites n₁ and n₂, the dynamics depend on a product of power laws, . Thus, two input signals which vary over time in an inverse way can lead to no response. When the two inputs affect two different receptors, other types of integration may be found and generally the system is not constrained to respond according to the product of the fold-change of each signal. These predictions can be readily tested experimentally, by providing cells with two simultaneously varying input signals. The present study suggests how cells can compare apples and oranges, namely by comparing each to its own background level, and then multiplying these two fold-changes.     

Molecular and cellular organization of insect chemosensory neurons

Animals use their chemosensory systems to detect and discriminate among chemical cues in the environment. Remarkable progress has recently been made in our knowledge of the molecular and cellular basis of chemosensory perception in insects, based largely on studies in Drosophila. This progress has been possible due to the identification of gene families for olfactory and gustatory receptors, the use of electro-physiological recording techniques on sensory neurons, the multitude of genetic manipulations that are available in this species, and insights from several insect model systems. Recent studies show that the superfamily of chemoreceptor proteins represent the essential elements in chemosensory coding, endowing chemosensory neurons with their abilities to respond to specific sets of odorants, tastants or pheromones. Investigating how insects detect chemicals in their environment can show us how receptor protein structures relate to ligand binding, how nervous systems process complex information, and how chemosensory systems and genes evolve.     

Establishing character correspondence for sensory organ traits in flies: sensory organ development provides insight for reconstructing character evolution

In Diptera and in other insects sensory organ patterns play an important role in the construction of phylogenies based on morphological characters. In this paper I explore the developmental basis for sensory organ pattern transformations between and within species. Knowledge of the properties of sensory organ development provides a foundation to judge the correspondence relationships between sensory organs. This is used to explore what components of notum bristle patterns are equivalent across the Schizophora. By investigating patterning processes in leg development, and their conservation across holometabolous insects, I show ways of relating specialised leg vestiture between species. Sensory organ patterns on the legs are diversified under homeotic gene control, potentially adding patterns of homeotic variation between legs to the list of informative traits for phylogenetic analysis. Correspondence relationships between wing and haltere sensory organ fields are resolved by exploring homeotic gene action in detail.     

Evolution of behavioural and cellular defences against parasitoid wasps in the Drosophila melanogaster subgroup

It may be intuitive to predict that host immune systems will evolve to counter a broad range of potential challenges through simultaneous investment in multiple defences. However, this would require diversion of resources from other traits, such as growth, survival and fecundity. Therefore, ecological immunology theory predicts that hosts will specialize in only a subset of possible defences. We tested this hypothesis through a comparative study of a cellular immune response and a putative behavioural defence used by eight fruit fly species against two parasitoid wasp species (one generalist and one specialist). Fly larvae can survive infection by melanotically encapsulating wasp eggs, and female flies can potentially reduce infection rates in their offspring by laying fewer eggs when wasps are present. The strengths of both defences varied significantly but were not negatively correlated across our chosen host species; thus, we found no evidence for a trade‐off between behavioural and cellular immunity. Instead, cellular defences were significantly weaker against the generalist wasp, whereas behavioural defences were similar in strength against both wasps and positively correlated between wasps. We investigated the adaptive significance of wasp‐induced oviposition reduction behaviour by testing whether wasp‐exposed parents produce offspring with stronger cellular defences, but we found no support for this hypothesis. We further investigated the sensory basis of this behaviour by testing mutants deficient in either vision or olfaction, both of which failed to reduce their oviposition rates in the presence of wasps, suggesting that both senses are necessary for detecting and responding to wasps.     

Sensory ecology and perceptual allocation: new prospects for neural networks

Sensory ecology provides a conceptual framework for considering how animals ought to design sensory systems to capture meaningful information from their environments. The framework has been particularly successful at describing how one should allocate sensory receptors to maximize performance on a given task. Neural networks, in contrast, have made unique contributions to understanding how 'hidden preferences' can emerge as a by-product of sensory design. The two frameworks comprise complementary techniques for understanding the design and the evolution of sensation. This article reviews empirical literature from multiple modalities and levels of sensory processing, considering vision, audition and touch from the viewpoints of sensory ecology and neuroethology. In the process, it presents modifications of extant neural network algorithms that would allow a more effective integration of these diverse approaches. Together, the reviewed literature suggests important advances that can be made by explicitly formulating neural network models in terms of sensory ecology, by incorporating neural costs into models of perceptual evolution and by exploring how such demands interact with historical forces.     

Ontogenetic shifts in olfactory rosette morphology of the sockeye salmon,Oncorhynchus nerka

Sockeye salmon, Oncorhynchus nerka, are anadromous, semelparous fish that breed in freshwater—typically in streams, and juveniles in most populations feed in lakes for 1 or 2 years, then migrate to sea to feed for 2 or 3 additional years, before returning to their natal sites to spawn and die. This species undergoes important changes in behavior, habitat, and morphology through these multiple life history stages. However, the sensory systems that mediate these migratory patterns are not fully understood, and few studies have explored changes in sensory function and specialization throughout ontogeny. This study investigates changes in the olfactory rosette of sockeye salmon across four different life stages (fry, parr, smolt, and adult). Development of the olfactory rosette was assessed by comparing total rosette size (RS), lamellae number, and lamellae complexity from scanning electron microscopy images across life stages, as a proxy for olfactory capacity. Olfactory RS increased linearly with lamellae number and body size (p < .001). The complexity of the rosette, including the distribution of sensory and nonsensory epithelia and the appearance of secondary lamellar folding, varied between fry and adult life stages. These differences in epithelial structure may indicate variation in odor-processing capacity between juveniles imprinting on their natal stream and adults using those odor memories in the final stages of homing to natal breeding sites. These findings improve our understanding of the development of the olfactory system throughout life in this species, highlighting that ontogenetic shifts in behavior and habitat may coincide with shifts in nervous system development.     

Olfactory receptor gene evolution is unusually rapid across Tetrapoda and outpaces chemosensory phenotypic change

Chemosensation is the most ubiquitous sense in animals, enacted by the products of complex gene families that detect environmental chemical cues and larger-scale sensory structures that process these cues. While there is a general conception that olfactory receptor (OR) genes evolve rapidly, the universality of this phenomenon across vertebrates, and its magnitude, are unclear. The supposed correlation between molecular rates of chemosensory evolution and phenotypic diversity of chemosensory systems is largely untested. We combine comparative genomics and sensory morphology to test whether OR genes and olfactory phenotypic traits evolve at faster rates than other genes or traits. Using published genomes, we identified ORs in 21 tetrapods, including amphibians, reptiles, birds, and mammals and compared their rates of evolution to those of orthologous non-OR protein-coding genes. We found that, for all clades investigated, most OR genes evolve nearly an order of magnitude faster than other protein-coding genes, with many OR genes showing signatures of diversifying selection across nearly all taxa in this study. This rapid rate of evolution suggests that chemoreceptor genes are in “evolutionary overdrive,” perhaps evolving in response to the ever-changing chemical space of the environment. To obtain complementary morphological data, we stained whole fixed specimens with iodine, µCT-scanned the specimens, and digitally segmented chemosensory and nonchemosensory brain regions. We then estimated phenotypic variation within traits and among tetrapods. While we found considerable variation in chemosensory structures, they were no more diverse than nonchemosensory regions. We suggest chemoreceptor genes evolve quickly in reflection of an ever-changing chemical space, whereas chemosensory phenotypes and processing regions are more conserved because they use a standardized or constrained architecture to receive and process a range of chemical cues.     

The ability of Drosophila hybrids to locate food declines with parental divergence

Hybrids are generally less fit than their parental species, and the mechanisms underlying their fitness reductions can manifest through different traits. For example, hybrids can have physiological, behavioral, or ecological defects, and these defects can generate reproductive isolation between their parental species. However, the rate that mechanisms of postzygotic isolation other than hybrid sterility and inviability evolve has remained largely uninvestigated, despite isolated studies showing that behavioral defects in hybrids are not only possible but might be widespread. Here, we study a fundamental animal behavior—the ability of individuals to find food—and test the rate at which it breaks down in hybrids. We measured the ability of hybrids from 94 pairs of Drosophila species to find food and show that this ability decreases with increasing genetic divergence between the parental species and that male hybrids are more strongly (and negatively) affected than females. Our findings quantify the rate that hybrid dysfunction evolves across the diverse radiation of Drosophila and highlights the need for future investigations of the genetic and neurological mechanisms that affect a hybrid's ability to find a suitable substrate on which to feed and breed.     

Elimination of sensory inputs induces growth and synaptic changes in crayfish motor axons

Damage to motor neurons induces regeneration processes including axonal growth and change of synaptic properties. Sensory axons that run along the motor axons are also damaged, but their possible role in the motor neuron''s regeneration is generally ignored. Here, the effect of eliminating some sensory inputs from intact motor axons on the motor axon''s properties was studied. Micro-dissecting one of the segmental, bilateral, sensory stretch receptor pairs of the crayfish abdomen induced the deep extensor abdominal motor axons to grow and changed their synaptic properties. The results demonstrate directly, probably for the first time, that change in sensory neuron activity can induce motor axons to grow, form new synapses, and change their synaptic properties.     

The systems analysis approach to mechanosensory coding

An important problem in neuroscience is to obtain quantitative knowledge of how information is represented, or encoded, in the signals that nerve cells process and transmit. Sensory receptors have provided important models for the study of neural coding because their inputs can often be relatively easily controlled and measured, while the resultant activity is recorded. A variety of engineering concepts have been successfully applied to physiological sciences, particularly those related to control of dynamic systems. Linear systems analysis was one of the earliest methods used to probe sensory coding, and measurements such as step responses and frequency responses have become standard tools for describing sensory functions. Modern systems analysis has evolved to provide accurate and efficient linear identification of encoding in sensory receptors that use either graded potentials or action potentials. It has also led to nonlinear systems analysis, the creation of parametric nonlinear models, and measures of information coding by sensory neurons. These methods promise to provide important new knowledge about sensory systems in the future, especially when complemented with parallel biophysical and molecular studies of sensory neurons. Mechanoreceptors provided some of the earliest preparations for the investigation of neural coding, and both the linear and nonlinear properties of wide variety of vertebrate and invertebrate mechanoreceptors continue to be explored. This article is part of a special issue on Neuronal Dynamics of Sensory Coding.     

Variability of spike trains and the processing of temporal patterns of acoustic signals—problems,constraints, and solutions

Object recognition and classification by sensory pathways is rooted in spike trains provided by sensory neurons. Nervous systems had to evolve mechanisms to extract information about relevant object properties, and to separate these from spurious features. In this review, problems caused by spike train variability and counterstrategies are exemplified for the processing of acoustic signals in orthopteran insects. Due to size limitations of their nervous system we expect to find solutions that are stripped to the computational basics. A key feature of auditory systems is temporal resolution, which is likely limited by spike train variability. Basic strategies to reduce such variability are to integrate over time, or to average across several neurons. The first strategy is constrained by its possible interference with temporal resolution. Grasshoppers do not seem to explore temporal integration much, in spite of the repetitive structure of their songs, which invites for multiple looks at the signal. The benefits of averaging across neurons depend on uncorrelated responses, a factor that may be crucial for the performance and evolution of small nervous systems. In spite of spike train variability the temporal information necessary for the recognition of conspecifics is preserved to a remarkable degree in the auditory pathway.Abbreviations dB decibel - CV coefficient of variation - SNR signal to noise ratio     

The neuroecology of competitor recognition

Territorial animals can be expected to distinguish among the types of competitors and noncompetitors that they encounter on a regular basis, including prospective mates and rivals of their own species, but they may not correctly classify individuals of other species. Closely related species often have similar phenotypes and this can cause confusion when formerly allopatric populations first come into contact. Errors in recognizing competitors can have important ecological and evolutionary effects. I review what is known about the mechanisms of competitor recognition in animals generally, focusing on cases in which the targets of recognition include other species. Case studies include damselflies, ants, skinks, salamanders, reef fishes, and birds. In general, recognition systems consist of a phenotypic cue (e.g., chemical, color, song), a neural template against which cues are compared, a motor response (e.g., aggression), and sensory integration circuits for context dependency of the response (if any). Little is known about how competitor recognition systems work at the neural level, but inferences about specificity of cues and about sensory integration can be drawn from the responses of territory residents to simulated intruders. Competitor recognition often involves multiple cues in the same, or different, sensory modalities. The same cues and templates are often, but not always, used for intraspecific and interspecific recognition. Experiments have shown that imprinting on local cues is common, which may enable templates to track evolved changes in cues automatically. The dependence of aggression and tolerance on context is important even in the simplest systems. Species in which mechanisms of competitor recognition are best known offer untapped opportunities to examine how competitor-recognition systems evolve (e.g., by comparing allopatric and sympatric populations). Cues that are gene products (peptides, proteins) may provide insights into rates of evolution. There are many avenues for further research on the important but understudied question of how animals recognize competitors.     

Plasticity of opsin gene expression in cichlids from Lake Malawi

Sensory systems play crucial roles in survival and reproduction. Therefore, sensory plasticity has important evolutionary implications. In this study, we examined retinal plasticity in five species of cichlid fish from Lake Malawi. We compared the cone opsin expression profiles of wild‐caught fish to lab‐reared F₁ that had been raised in a UV minus, reduced intensity light environment. All of the opsin genes that were expressed in wild‐caught fish were also expressed in lab‐reared individuals. However, we found statistically significant differences in relative opsin expression among all five species. The most consistent difference was in the SWS2B (violet) opsin, which was always expressed at higher levels in lab‐reared individuals. Estimates of visual pigment quantum catch suggest that this change in expression would increase retinal sensitivity in the light environment of the lab. We also found that the magnitude of plasticity varied across species. These findings have important implications for understanding the genetic regulation of opsin expression and raise many interesting questions about how the cichlid visual system develops. They also suggest that sensory plasticity may have facilitated the ecological diversification of cichlids in Lake Malawi.     

THERMAL PERCEPTIONS AND PREFERENCES IN INDOOR ENVIRONMENTS

Sensory analysis was applied to the study of thermal perception, in order to determine and characterize end‐users’ preferences concerning five indoor thermal environments generated by different heating systems. In this review, we developed a sensory profile method to describe and quantify the sensory characteristics of the thermal environments. A consumer test was also performed in order to investigate the hedonic judgment of 119 end users. The results show that trained assessors are able to describe and quantify sensory differences between the environments with high reliability. Consumers’ preferences are influenced by both their thermal sensations in the environments, as expressed by the sensory panel, and their personal opinions of the corresponding heating systems.