Evolution of sensory systems

Sensory systems evolve and enable organisms to perceive their sensory Umwelt, the unique set of cues relevant for their survival. The multiple components that comprise sensory systems — the receptors, cells, organs, and dedicated high-order circuits — can vary greatly across species. Sensory receptor gene families can expand and contract across lineages, resulting in enormous sensory diversity. Comparative studies of sensory receptor function have uncovered the molecular basis of receptor properties and identified novel sensory receptor classes and noncanonical sensory strategies. Phylogenetically informed comparisons of sensory systems across multiple species can pinpoint when sensory changes evolve and highlight the role of contingency in sensory system evolution.     

Ultrastructure of sensory cells on the mantle tentacles of the gastropod Notoacmea scutum

Previous studies have indicated that the mantle margin of the gastropod mollusc Notoacmea scutum is sensitive to chemical, photic, and mechanical stimulation. Here, the ultrastructure of sensory cells on the mantle tentacles of N. scutum is examined by transmission electron microscopy to determine if morphological types of sensory cells can be correlated with known sensory capabilities. The sensory cells of the mantle tentacles are found to be ciliated, primary receptors with subepithelial nuclei. The ciliated sensory endings are concentrated at the tip of the tentacles, but also occur in smaller numbers along the shaft. Ultrastructural differences between cilia form the basis of distinguishing two types of sensory ending. Type 1 sensory endings, which are over 90% of the endings, bar unusual cilia that typically are filled with an electron-dense material. Type 2 sensory endings bear cilia that have a 9 + 2 arrangement of longitudinal elements and thus more closely resemble previously reported sensory cilia of molluscs.     

Biases in signal evolution: learning makes a difference

It is now well established that signal receivers have a key role in the evolution of animal communication: the suite of sensory and cognitive processes by which animals perceive and learn about their environment can have a significant impact on signal design. A crucial property of these information-processing mechanisms is the emergence of 'receiver bias' in the behavioural responses to signals. Whereas most research has focussed on receiver biases in the sensory system, more recent studies show that biases can also arise from learning about signals. Here, we highlight how learning-based biases can arise, and how these differ from biases emerging from sensory systems in their impact on signal evolution.     

Cannabinoid modulation of sensory neurotransmission via cannabinoid and vanilloid receptors: roles in regulation of cardiovascular function

Capsaicin-sensitive sensory nerves are widely distributed in the cardiovascular system. They are activated by a variety of physical and chemical stimuli, characteristically by capsaicin acting via the vanilloid receptor VR1, and have a role in the regulation of peripheral vascular resistance and maintenance of homeostasis via their afferent and efferent functions. Cannabinoids, a recently discovered family of extracellular signalling molecules, can act at cannabinoid (CB) receptors expressed on sensory nerves, to cause inhibition of sensory neurotransmitter release. There is recent evidence, however, that anandamide, an endogenous cannabinoid, can activate VR1, coexpressed with CB receptors on the same sensory nerve terminals, causing a release of sensory neurotransmitter, vasorelaxation and hypotension. Hence, anandamide can elicit opposite actions, inhibition via CB receptors and excitation via VR1, on sensory neurotransmission. The possible biological significance of this is discussed.     

Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance

Anthropogenic sensory pollution is affecting ecosystems worldwide. Human actions generate acoustic noise, emanate artificial light and emit chemical substances. All of these pollutants are known to affect animals. Most studies on anthropogenic pollution address the impact of pollutants in unimodal sensory domains. High levels of anthropogenic noise, for example, have been shown to interfere with acoustic signals and cues. However, animals rely on multiple senses, and pollutants often co-occur. Thus, a full ecological assessment of the impact of anthropogenic activities requires a multimodal approach. We describe how sensory pollutants can co-occur and how covariance among pollutants may differ from natural situations. We review how animals combine information that arrives at their sensory systems through different modalities and outline how sensory conditions can interfere with multimodal perception. Finally, we describe how sensory pollutants can affect the perception, behaviour and endocrinology of animals within and across sensory modalities. We conclude that sensory pollution can affect animals in complex ways due to interactions among sensory stimuli, neural processing and behavioural and endocrinal feedback. We call for more empirical data on covariance among sensory conditions, for instance, data on correlated levels in noise and light pollution. Furthermore, we encourage researchers to test animal responses to a full-factorial set of sensory pollutants in the presence or the absence of ecologically important signals and cues. We realize that such approach is often time and energy consuming, but we think this is the only way to fully understand the multimodal impact of sensory pollution on animal performance and perception.     

Neural processing as causal inference

Perception is about making sense, that is, understanding what events in the outside world caused the sensory observations. Consistent with this intuition, many aspects of human behavior confronting noise and ambiguity are well explained by principles of causal inference. Extending these insights, recent studies have applied the same powerful set of tools to perceptual processing at the neural level. According to these approaches, microscopic neural structures solve elementary probabilistic tasks and can be combined to construct hierarchical predictive models of the sensory input. This framework suggests that variability in neural responses reflects the inherent uncertainty associated with sensory interpretations and that sensory neurons are active predictors rather than passive filters of their inputs. Causal inference can account parsimoniously and quantitatively for non-linear dynamical properties in single synapses, single neurons and sensory receptive fields.     

Exploring developmental, functional, and evolutionary aspects of amphioxus sensory cells

Amphioxus has neither elaborated brains nor definitive sensory organs, so that the two may have evolved in a mutually affecting manner and given rise to the forms seen in extant vertebrates. Clarifying the developmental and functional aspects of the amphioxus sensory system is thus pivotal for inferring the early evolution of vertebrates. Morphological studies have identified and classified amphioxus sensory cells; however, it is completely unknown whether the morphological classification makes sense in functional and evolutionary terms. Molecular markers, such as gene expression, are therefore indispensable for investigating the developmental and functional aspects of amphioxus sensory cells. This article reviews recent molecular studies on amphioxus sensory cells. Increasing evidence shows that the non-neural ectoderm of amphioxus can be subdivided into molecularly distinct subdomains by the combinatorial code of developmental cues involving the RA-dependent Hox code, suggesting that amphioxus epithelial sensory cells developed along positional information. This study focuses particularly on research involving the molecular phylogeny and expression of the seven-transmembrane, G protein-coupled receptor (GPCR) genes and discusses the usefulness of this information for characterizing the sensory cells of amphioxus.     

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.     

Is there a role for T-type calcium channels in peripheral and central pain sensitization?

Following tissue injury, both peripheral and central sensory neurons can become hyperexcitable, or “sensitized.” Sensitization can lead to long-term pathological changes in pain sensation. Because many chronic pain conditions are refractory to most currently available treatments, there is great interest in identifying molecular targets that contribute to the sensitization of sensory neurons. Among these, several classes of ion channels have emerged as potential targets. Recent in vitro and in vivo studies have demonstrated a role for T-type Ca²⁺ channels in sensory pathways and have suggested that these channels may contribute to pain processing and sensitization. Therefore, T-type channels may represent an opportunity for the development of novel pain therapeutics and may help to address an unmet medical need.     

Sensory activity affects sensory axon development in C. elegans

The simple nervous system of the nematode C. elegans consists of 302 neurons with highly reproducible morphologies, suggesting a hard-wired program of axon guidance. Surprisingly, we show here that sensory activity shapes sensory axon morphology in C. elegans. A class of mutants with deformed sensory cilia at their dendrite endings have extra axon branches, suggesting that sensory deprivation disrupts axon outgrowth. Mutations that alter calcium channels or membrane potential cause similar defects. Cell-specific perturbations of sensory activity can cause cell-autonomous changes in axon morphology. Although the sensory axons initially reach their targets in the embryo, the mutations that alter sensory activity cause extra axon growth late in development. Thus, perturbations of activity affect the maintenance of sensory axon morphology after an initial pattern of innervation is established. This system provides a genetically tractable model for identifying molecular mechanisms linking neuronal activity to nervous system structure.     

Learning to hear: plasticity of auditory cortical processing

Sensory experience and auditory cortex plasticity are intimately related. This relationship is most striking during infancy when changes in sensory input can have profound effects on the functional organization of the developing cortex. But a considerable degree of plasticity is retained throughout life, as demonstrated by the cortical reorganization that follows damage to the sensory periphery or by the more controversial changes in response properties that are thought to accompany perceptual learning. Recent studies in the auditory system have revealed the remarkably adaptive nature of sensory processing and provided important insights into the way in which cortical circuits are shaped by experience and learning.     

Biomimetic vibrissal sensing for robots

Active vibrissal touch can be used to replace or to supplement sensory systems such as computer vision and, therefore, improve the sensory capacity of mobile robots. This paper describes how arrays of whisker-like touch sensors have been incorporated onto mobile robot platforms taking inspiration from biology for their morphology and control. There were two motivations for this work: first, to build a physical platform on which to model, and therefore test, recent neuroethological hypotheses about vibrissal touch; second, to exploit the control strategies and morphology observed in the biological analogue to maximize the quality and quantity of tactile sensory information derived from the artificial whisker array. We describe the design of a new whiskered robot, Shrewbot, endowed with a biomimetic array of individually controlled whiskers and a neuroethologically inspired whisking pattern generation mechanism. We then present results showing how the morphology of the whisker array shapes the sensory surface surrounding the robot's head, and demonstrate the impact of active touch control on the sensory information that can be acquired by the robot. We show that adopting bio-inspired, low latency motor control of the rhythmic motion of the whiskers in response to contact-induced stimuli usefully constrains the sensory range, while also maximizing the number of whisker contacts. The robot experiments also demonstrate that the sensory consequences of active touch control can be usefully investigated in biomimetic robots.     

Ring-shaped organization of cytoskeletal F-actin associated with surface sensory receptors of Schistosoma mansoni: a confocal and electron microscopic study

The surface syncytial epithelium of the human blood fluke, Schistosoma mansoni, contains numerous ciliated or unciliated, bulb-shaped sensory receptors. At the ultrastructure level, sensory receptors with similar topographic and morphological structures have been found in the epithelial surface layers of all known species of schistosomes and other species of flatworm parasites. Although many studies have focused on the syncytial cytoskeleton of schistosomes, while some other studies have examined the fine structures of the syncytial sensory receptors, no-one has demonstrated the association of cytoskeletal elements with the surface sensory cells except the well-known microtubules associated with ciliated structures. The present study, using confocal laser scanning microscopy combined with scanning and transmission electron microscopies, demonstrates the association of ring-shaped F-actin within the epithelial sensory receptors. The F-actin rings can be characterized into two types according to their size, density, and distribution. The actin rings found in the syncytia of both the male and female schistosomes appear to be more dense and larger in size than the actin rings located only at the central regions of the tuberculated structures of the male dorsal syncytium. Our observation of F-actin rings associated with the spine-bearing tubercles, combined with the results obtained from other ultrastructural investigations, also indicate the presence of the unciliated sensory receptors in each tuberculated structure of the male dorsal surface syncytium, which have not been reported in other studies on schistosome epithelial sensory cells.     

Neural correlates of categories and concepts

The ability to readily adapt to novel situations requires something beyond storing specific stimulus-response associations. Instead, many animals can detect basic characteristics of events and store them as generalized classes. Because these representations are abstracted beyond specific details of sensory inputs and motor outputs, they can be easily generalized and adapted to new circumstances. Explorations of neural mechanisms of sensory processing and motor output have progressed to the point where studies can begin to address the neural basis of abstract, categorical representations. Recent studies have revealed their neural correlates in various cortical areas of the non-human primate brain.     

Sensory gating and its modulation by cannabinoids: electrophysiological, computational and mathematical analysis

Gating of sensory information can be assessed using an auditory conditioning-test paradigm which measures the reduction in the auditory evoked response to a test stimulus following an initial conditioning stimulus. Recording brainwaves from specific areas of the brain using multiple electrodes is helpful in the study of the neurobiology of sensory gating. In this paper, we use such technology to investigate the role of cannabinoids in sensory gating in the CA3 region of the rat hippocampus. Our experimental results show that application of the exogenous cannabinoid agonist WIN55,212-2 can abolish sensory gating. We have developed a phenomenological model of cannabinoid dynamics incorporated within a spiking neural network model of CA3 with synaptically interacting pyramidal and basket cells. Direct numerical simulations of this model suggest that the basic mechanism for this effect can be traced to the suppression of inhibition of slow GABA_B synapses. Furthermore, by working with a simpler mathematical firing rate model we are able to show the robustness of this mechanism for the abolition of sensory gating.     

Shifting baselines in attention research

Psychophysical and physiological studies have shown that attending to a stimulus can enhance its sensory processing. Functional imaging studies now reveal that attention can also modulate activity in sensory brain areas before stimulus onset, when the observer prepares to attend to an anticipated stimulus. These preparatory 'baseline shifts' in brain activity pose many new questions, and potentially offer new insights into the neural basis of perceptual awareness.     

Transplantation of neurons reveals processing areas and rules for synaptic connectivity in the cricket nervous system

In order to assess the nature of spatial cues in determining the characteristic projection sites of sensory neurons in the CNS, we have transplanted sensory neurons of the cricket Acheta domesticus to ectopic locations. Thoracic campaniform sensilla (CS) function as proprioceptors and project to an intermediate layer of neuropil in thoracic ganglia while cercal CS transduce tactile information and project into a ventral layer in the terminal abdominal ganglion (TAG). When transplanted to ectopic locations, these afferents retain their modality-specific projection in the host ganglion and terminate in the layer of neuropil homologous to that of their ganglion of origin. Thus, thoracic CS neurons project to intermediate neuropil when transplanted to the abdomen and cercal CS neurons project to a ventral layer of neuropil when transplanted to the thorax. We conclude that CS can be separated into two classes based on their characteristic axonal projections within each segmental ganglion. We also found that the sensory neurons innervating tactile hairs project to ventral neuropil in any ganglion they encounter after transplantation. Ectopic sensory neurons can form functional synaptic connections with identified interneurons located within the host ganglia. The new contacts formed by these ectopic sensory neurons can be with normal targets, which arborize within the same layer of neuropil in each segmental ganglion, or with novel targets, which lack dendrites in the normal ganglion and are thus normally unavailable for synaptogenesis. These observations suggest that a limited set of molecular markers are utilized for cell–cell recognition in each segmentally homologous ganglion. Regenerating sensory neurons can recognize novel postsynaptic neurons if they have dendrites in the appropriate layer of neuropil. We suggest that spatial constraints produced by the segmentation and the modality-specific layering of the nervous system have a pivotal role in determining synaptic specificity. © 1993 John Wiley & Sons, Inc.     

A Normalization Model of Attentional Modulation of Single Unit Responses

Although many studies have shown that attention to a stimulus can enhance the responses of individual cortical sensory neurons, little is known about how attention accomplishes this change in response. Here, we propose that attention-based changes in neuronal responses depend on the same response normalization mechanism that adjusts sensory responses whenever multiple stimuli are present. We have implemented a model of attention that assumes that attention works only through this normalization mechanism, and show that it can replicate key effects of attention. The model successfully explains how attention changes the gain of responses to individual stimuli and also why modulation by attention is more robust and not a simple gain change when multiple stimuli are present inside a neuron''s receptive field. Additionally, the model accounts well for physiological data that measure separately attentional modulation and sensory normalization of the responses of individual neurons in area MT in visual cortex. The proposal that attention works through a normalization mechanism sheds new light a broad range of observations on how attention alters the representation of sensory information in cerebral cortex.