Sensory Systems

American gymnotiformes and African mormyriformes have evolved an active sensory system using a self-generated electric field as a carrier of signals. Objects polarized by the discharge of a specialized electric organ project their images on the skin where electroreceptors tuned to the time course of the self-generated field transduce local signals carrying information about impedance, shape, size, and location of objects, as well as electrocommunication messages, and encode them as primary afferents trains of spikes. This system is articulated with other cutaneous systems (passive electroreception and mechanoception) as well as proprioception informing the shape of the fish’s body. Primary afferents project on the electrosensory lobe where electrosensory signals are compared with expectation signals resulting from the integration of recent past electrosensory, other sensory, and, in the case of mormyriformes, electro- and skeleton-motor corollary discharges. This ensemble of signals converges on the apical dendrites of the principal cells where a working memory of the recent past, and therefore predictable input, is continuously built up and updated as a pattern of synaptic weights. The efferent neurons of the electrosensory lobe also project to the torus and indirectly to other brainstem nuclei that implement automatic electro- and skeleton-motor behaviors. Finally, the torus projects via the preglomerular nucleus to the telencephalon where cognitive functions, including “electroperception” of shape-, size- and impedance-related features of objects, recognition of conspecifics, perception based decisions, learning, and abstraction, are organized.

Decreased ability to smell is common in older persons. Some demonstrable smell loss is present in more than 50% of those 65 to 80 years of age, with up to 10% having no smell at all (anosmia). Over the age of 80, 75% exhibit some loss with up to 20% being totally anosmic. The causes of these decrements appear multifactorial and likely include altered intranasal airflow patterns, cumulative damage to the olfactory receptor cells from viruses and other environmental insults, decrements in mucosal metabolizing enzymes, closure of the cribriform plate foramina through which olfactory receptor cells axons project to the brain, loss of selectivity of receptor cells to odorants, and altered neurotransmission, including that exacerbated in some age-related neurodegenerative diseases.

Gustatory signals from the mouth travel to the rostral nucleus of the solitary tract (rNST) over the VIIth (anterior tongue and palate) and IXth (posterior tongue) cranial nerves and synapse in the central subdivision in an overlapping orotopic pattern. Oral somatosensory information likewise reaches rNST, preferentially terminating in the lateral subdivision. Two additional rNST subdivisions, the medial and ventral, receive only sparse primary afferent inputs. Ascending pathways arise primarily from the central subdivision; local reflex and intranuclear pathways originate from the other subdivisions. Thus, parallel processing is already evident at the first central nervous system (CNS) relay. Ascending rNST taste fibers connect to the pontine parabrachial nucleus (PBN), strongly terminating in the ventral lateral (VL) and medial subnuclei (M) of the waist region but also in the external lateral (EL) and medial (EM) subnuclei. PBN projections travel along two main routes. A “lemniscal” processing stream connects to the thalamic taste relay, the parvicellular division of the ventroposteromedial nucleus (VPMpc), which in turn projects to insular cortex. A second, “limbic” pathway synapses in the lateral hypothalamus (LH), central nucleus of the amygdala (CeA), bed nucleus of the stria terminalis (BNST), and substantia innominata (SI). The ventral tegmental area (VTA), a critical nucleus in the so-called reward circuit, also receives input from the gustatory PBN. Forebrain gustatory structures are interconnected and give rise to copious feedback pathways. Single-neuron recording and calcium imaging demonstrates that taste response profiles in both the peripheral nerves and CNS lemniscal structures are highly orderly. Arguably, a limited number of neuron “types” are defined by the qualitative class of compounds (sugars, sweeteners, amino acids, sodium salts, acids and non-sodium salts, “bitter”) that elicit the largest response in a cell. In the periphery and NST, some findings suggest these classes correspond to distinct molecular phenotypes and functions, but evidence for a cortical chemotopic organization is highly controversial. CNS neuron types are complicated by convergence and lability as a function of homeostatic, cognitive, and experiential variables. Moreover, gustatory responses are dynamic, providing additional coding potential in the temporal domain. Interestingly, taste responses in the limbic pathway are particularly plastic and code for hedonics more obviously than quality. Studies in decerebrate rats reveal that the brainstem is sufficient to maintain appropriate oromotor and somatic responses, referred to as taste reactivity, to nutritive (sugars) and harmful (quinine) stimuli. However, forebrain processing is necessary for taste reactivity to be modulated by learning, at least with respect to taste aversion conditioning. Functional studies of the rodent cortex tell a complex story. Lesion studies in rats emphasize a considerable degree of residual function in animals lacking large regions of insular cortex despite demonstrating shifts in detection thresholds for certain, but not all, stimuli representing different taste qualities. They also have an impact on conditioned taste aversion. Investigations in mice employing optogenetic and chemogenetic manipulations suggest that different regions of insular cortex are critical for discriminating certain qualities and that their connections to the amygdala underlie their hedonic impact. The continued use of sophisticated behavioral experiments coordinated with molecular methods for monitoring and manipulating activity in defined neural circuits should ultimately yield satisfying answers to long-standing debates about the fundamental operation of the gustatory system.

Annelid worms are simultaneously an interesting and difficult model system for understanding the evolution of animal vision. On the one hand, a wide variety of photoreceptor cells and eye morphologies are exhibited within a single phylum; on the other, annelid phylogenetics has been substantially re-envisioned within the last decade, suggesting the possibility of considerable convergent evolution. This article reviews the comparative anatomy of annelid visual systems within the context of the specific behaviors exhibited by these animals. Each of the major classes of annelid visual systems is examined, including both simple photoreceptor cells (including leech body eyes) and photoreceptive cells with pigment (trochophore larval eyes, ocellar tubes, complex eyes); meanwhile, behaviors examined include differential mobility and feeding strategies, similarities (or differences) in larval versus adult visual behaviors within a species, visual signaling, and depth sensing. Based on our review, several major trends in the comparative morphology and ethology of annelid vision are highlighted: (1) eye complexity tends to increase with mobility and higher-order predatory behavior; (2) although they have simple sensors these can relay complex information through large numbers or multimodality; (3) polychaete larval and adult eye morphology can differ strongly in many mobile species, but not in many sedentary species; and (4) annelids exhibiting visual signaling possess even more complex visual systems than expected, suggesting the possibility that complex eyes can be simultaneously well adapted to multiple visual tasks.

The organs of the vertebrate inner ear respond to a variety of mechanical stimuli: semicircular canals are sensitive to angular velocity, the saccule and utricle respond to linear acceleration (including gravity), and the cochlea is sensitive to airborne vibration, or sound. The ontogenically related lateral line organs, spaced along the sides of aquatic vertebrates, sense water movement. All these organs have a common receptor cell type, which is called the hair cell, for the bundle of enlarged microvilli protruding from its apical surface. In different organs, specialized accessory structures serve to collect, filter, and then deliver these physical stimuli to the hair bundles. The proximal stimulus for all hair cells is deflection of the mechanosensitive hair bundle. Hair cells convert mechanical information contained within the temporal pattern of hair bundle deflections into electrical signals, which they transmit to the brain for interpretation.

Age-related hearing loss affects over half of the elderly population, yet it remains poorly understood. Natural aging can cause the input to the brain from the cochlea to be progressively compromised in most individuals, but in many cases the cochlea has relatively normal sensitivity and yet people have an increasingly difficult time processing complex auditory stimuli. The two main deficits are in sound localization and temporal processing, which lead to poor speech perception. Animal models have shown that there are multiple changes in the brainstem, midbrain, and thalamic auditory areas as a function of age, giving rise to an alteration in the excitatory/inhibitory balance of these neurons. This alteration is manifest in the cerebral cortex as higher spontaneous and driven firing rates, as well as broader spatial and temporal tuning. These alterations in cortical responses could underlie the hearing and speech processing deficits that are common in the aged population.

Understanding of the various types of plasticity that occur in the spinal cord, as well as understanding of spinal cord functions, has vastly improved over the past 50 years, mainly due to an increase in the number of research studies and review articles on the subject. It is now understood that the spinal cord is not merely a passive conduit of neural impulses. Instead, the spinal cord can independently execute complex functions. Numerous experimental approaches have been utilized for more targeted exploration of spinal cord functions. For example, isolating the spinal cord from supraspinal influences has been used to demonstrate that simple forms of learning can be performed by spinal neuronal networks. Moreover, reduced preparations, such as acute spinal cord slices, have been used to show that spinal neurons undergo different types of modulation, including activity-dependent synaptic modification. Most spinal cord processes, ranging from integration of incoming sensory input to execution of locomotor outputs, involve plasticity. Nociceptive processing that leads to pain and spinal learning is an example of plasticity that is well-studied in the spinal cord. At the neural level, both processes involve an interplay of cellular mediators, which include glutamate receptors, protein kinases, and growth factors. The neurotrophin brain-derived neurotrophic factor (BDNF) has also been implicated in these processes, specifically as a promoter of both pro-nociception and spinal learning mechanisms. Interestingly, the role of BDNF in mediating spinal plasticity can be altered by injury. The literature spanning approximately 5 decades is reviewed and the role of BDNF is discussed in mediating cellular plasticity underlying pain processing and learning within the spinal cord.

Toothed whales and dolphins, odontocete cetaceans, produce very loud biosonar sounds in order to navigate and to locate and catch their prey of fish and squid. Underwater biosonar was not discovered until after 1950, but the initial experiments demonstrated a unique sensory modality that could find small targets far away and distinguish between objects buried in mud that differed only by the metal from which they were made. Dolphins determine the distance to their prey by evaluating very small time differences between the outgoing signal and the echo return. The type of outgoing signal varies greatly from low frequency, explosively loud sperm whale clicks, to frequency modulated mid-frequency beaked whale sounds, to very high frequency (over 100 kHz) harbor porpoise signals. All appear to be made by specialized pneumatic phonic lips closely connected to sound projecting fatty melons that focus sound before sending out narrow echolocation sound beams. The frequency of most hearing is matched to echolocation, with the areas of best hearing of the animals being the areas of principal outgoing signal frequency. The sensation levels of hearing are under the animal’s control with “automatic gain control” operating to assure the best hearing of the echo returns. Angular localization of the bottlenose dolphins, for discriminating the minimum audible angles of clicks, is less than one degree in both the horizontal and vertical directions. This remarkable localization performance has yet to be fully explained, but new hypotheses of gular pathways, shaded receiver models, and internal pinnae may provide some explanations as a theory of auditory localization in the odontocetes develops.

Since the early 1980s, evidence suggesting that the vertebrate brain is a rich source of steroid hormones has been decisive and extensive. This evidence includes data from many vertebrate species and describes almost every enzyme necessary for the conversion of cholesterol to androgens and estrogens. In contrast, the behavioral relevance of neurosteroidogenesis is more equivocal and mysterious. Nonetheless, the presence of a limited number of steroidogenic enzymes in the brain of a few species has clearly been linked to reliable behavioral phenotype.

To survive, animals must properly sense their surrounding environment. The types of sensation that allow for detecting these changes can be categorized as tactile, thermal, aural, or olfactory. Olfaction is one of the most primitive senses, involving the detection of environmental chemical cues. Organisms must sense and discriminate between abiotic and biogenic cues, necessitating a system that can react and respond to changes quickly. The nematode, Caenorhabditis elegans, offers a unique set of tools for studying the biology of olfactory sensation. The olfactory system in C. elegans is comprised of 14 pairs of amphid neurons in the head and two pairs of phasmid neurons in the tail. The male nervous system contains an additional 89 neurons, many of which are exposed to the environment and contribute to olfaction. The cues sensed by these olfactory neurons initiate a multitude of responses, ranging from developmental changes to behavioral responses. Environmental cues might initiate entry into or exit from a long-lived alternative larval developmental stage (dauer), or pheromonal stimuli may attract sexually mature mates, or repel conspecifics in crowded environments. C. elegans are also capable of sensing abiotic stimuli, exhibiting attraction and repulsion to diverse classes of chemicals. Unlike canonical mammalian olfactory neurons, C. elegans chemosensory neurons express more than one receptor per cell. This enables detection of hundreds of chemical structures and concentrations by a chemosensory nervous system with few cells. However, each neuron detects certain classes of olfactory cues, and, combined with their synaptic pathways, elicit similar responses (i.e., aversive behaviors). The functional architecture of this chemosensory system is capable of supporting the development and behavior of nematodes in a manner efficient enough to allow for the genus to have a cosmopolitan distribution.

When one talks about hearing, some may first imagine the auricle (or external ear), which is the only visible part of the auditory system in humans and other mammals. Its shape and size vary among people, but it does not tell us much about a person’s abilities to hear (except perhaps their ability to localize sounds in space, where the shape of the auricle plays a certain role). Most of what is used for hearing is inside the head, particularly in the brain. The inner ear transforms mechanical vibrations into electrical signals; then the auditory nerve sends these signals into the brainstem, where intricate preprocessing occurs. Although auditory brainstem mechanisms are an important part of central auditory processing, it is the processing taking place in the cerebral cortex (with the thalamus as the mediator), which enables auditory perception and cognition. Human speech and the appreciation of music can hardly be imagined without a complex cortical network of specialized regions, each contributing different aspects of auditory cognitive abilities. During the evolution of these abilities in higher vertebrates, especially birds and mammals, the cortex played a crucial role, so a great deal of what is referred to as central auditory processing happens there. Whether it is the recognition of one’s mother’s voice, listening to Pavarotti singing or Yo-Yo Ma playing the cello, hearing or reading Shakespeare’s sonnets, it will evoke electrical vibrations in the auditory cortex, but it does not end there. Large parts of frontal and parietal cortex receive auditory signals originating in auditory cortex, forming processing streams for auditory object recognition and auditory-motor control, before being channeled into other parts of the brain for comprehension and enjoyment.

Chemoreception is the physiological capacity whereby organisms detect the varied external and internal chemical information required for survival and is the most primitive sensory process. Fish living in water have respiratory, gustatory, and olfactory chemosensory systems that detect water-soluble chemical cues. Respiratory chemoreception mainly in the gills detects changes in the levels of three respiratory gases: oxygen (O2), carbon dioxide (CO2), and ammonia (NH3). Gustatory chemoreception (gustation), which involves several taste receptor genes, is primarily involved in the tasting of foods. Olfactory chemoreception (olfaction), which involves between 15 and 150 olfactory receptor genes, is involved in a variety of important biological functions such as procuring foods, recognizing hazards (predators, contaminants, and toxic and alarm substances), discriminating species (individual, kin, and conspecific), controlling social behavior (dominance hierarchies, symbiotic behavior, territorial behavior, and schooling behavior), and reproductive and migratory behavior (mating, search for spawning site, imprinting, and homing). The olfactory functions are primarily controlled by hormones secreted from various endocrine glands that are the key mediators and integrators of external and internal information in organisms. Conversely, olfactory stimuli cause changes in hormone conditions. One good example is the amazing olfactory abilities of salmon. They can memorize information related to their natal stream odors during downstream migration in juveniles so that, after they travel thousands of kilometers in the ocean over many years during feeding migration, they are able to use their homing abilities to migrate precisely to their natal stream for reproduction in adults. Olfactory memory formation and retrieval of natal stream odors in salmon, which are primarily controlled by the brain–pituitary–thyroid hormones and brain–pituitary–gonad hormones, respectively, are essential to imprinting and homing migration. Salmon olfactory systems can discriminate seasonally and yearly stable compositions of dissolved amino acids in their natal streams produced by biofilms in the riverbed. Ocean and freshwater ecosystems may have been affected by climate change-related CO2-induced acidification that impairs olfactory-mediated neural and behavioral responses in fish.

The human brain processes noisy information to help make adaptive choices under uncertainty. Accompanying these decisions about incoming evidence is a sense of confidence: a feeling about whether a decision is correct. Confidence typically covaries with the accuracy of decisions, in that higher confidence is associated with higher decisional accuracy. In the laboratory, decision confidence is typically measured by asking participants to make judgments about stimuli or information (type 1 judgments) and then to rate their confidence on a rating scale or by engaging in wagering (type 2 judgments). The correspondence between confidence and accuracy can be quantified in a number of ways, some based on probability theory and signal detection theory. But decision confidence does not always reflect only the probability that a decision is correct; confidence can also reflect many other factors, including other estimates of noise, evidence magnitude, nearby decisions, decision time, and motor movements. Confidence is thought to be computed by a number of brain regions, most notably areas in the prefrontal cortex. And, once computed, confidence can be used to drive other behaviors, such as learning rates or social interaction.

Odorants, inhaled through the nose or exhaled from the mouth through the nose, bind to receptors on olfactory sensory neurons. Olfactory sensory neurons project in a highly stereotyped fashion into the forebrain to a structure called the olfactory bulb, where odorant-specific spatial patterns of neural activity are evoked. These patterns appear to reflect the molecular features of the inhaled stimulus. The olfactory bulb, in turn, projects to the olfactory cortex, which is composed of multiple sub-units including the anterior olfactory nucleus, the olfactory tubercle, the cortical nucleus of the amygdala, the anterior and posterior piriform cortex, and the lateral entorhinal cortex. Due to differences in olfactory bulb inputs, local circuitry and other factors, each of these cortical sub-regions appears to contribute to different aspects of the overall odor percept. For example, there appears to be some spatial organization of olfactory bulb inputs to the cortical nucleus of the amygdala, and this region may be involved in the expression of innate odor hedonic preferences. In contrast, the olfactory bulb projection to the piriform cortex is highly distributed and not spatially organized, allowing the piriform to function as a combinatorial, associative array, producing the emergence of experience-dependent odor-objects (e.g., strawberry) from the molecular features extracted in the periphery. Thus, the full perceptual experience of an odor requires involvement of a large, highly dynamic cortical network.

Olfactory systems are tasked with converting the chemical environment into electrical signals that the brain can use to optimize behaviors such as navigating towards resources, finding mates, or avoiding danger. Drosophila melanogaster has long served as a model system for several attributes of olfaction. Such features include sensory coding, development, and the attempt to link sensory perception to behavior. The strength of Drosophila as a model system for neurobiology lies in the myriad of genetic tools made available to the experimentalist, and equally importantly, the numerical reduction in cell numbers within the olfactory circuit. Modern techniques have recently made it possible to target nearly all cell types in the antennal lobe to directly monitor their physiological activity or to alter their expression of endogenous proteins or transgenes.

The neocortex is a part of the forebrain of mammals that is an innovation of mammal-like “reptilian” synapsid ancestors of early mammals. This neocortex emerged from a small region of dorsal cortex that was present in earlier ancestors and is still found in the forebrain of present-day reptiles. Instead of the thick structure of six layers of cells (five layers) and fibers (one layer) of neocortex of mammals, the dorsal cortex was characterized by a single layer of pyramidal neurons and a scattering of small, largely inhibitory neurons. In reptiles, the dorsal cortex is dominated by visual inputs, with outputs that relate to behavior and memory. The thicker neocortex of six layers in early mammals was already divided into a number of functionally specialized zones called cortical areas that were predominantly sensory in function, while relating to important aspects of motor behavior via subcortical projections. These early sensorimotor areas became modified in various ways as different branches of the mammalian radiation evolved, and neocortex often increased in size and the number of cortical areas, likely by the process of specializations within areas that subdivided areas. At least some areas, perhaps most, subdivided in another way by evolving two or more alternating types of small regions of different functional specializations, now referred to as cortical modules or columns. The specializations within and across cortical areas included those in the sizes of neurons and the extents of their processes, the dendrites and axons, and thus connections with other neurons. As a result, the neocortex of present-day mammals varies greatly within and across phylogenetically related groups (clades), while retaining basic features of organization from early ancestral mammals. In a number of present-day (extant) mammals, brains are relatively small and have little neocortex, with few areas and little structural differentiation, thus resembling early mammals. Other small mammals with little neocortex have specialized some part via selective enlargement and structural modifications to promote certain sensory abilities. Other mammals have a neocortex that is moderately to greatly expanded, with more cortical areas directly related to sensory processing and cognition and memory. The human brain is extreme in this way by having more neocortex in proportion to the rest of the brain, more cortical neurons, and likely more cortical areas.