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- Neuroscience x
James W. Grau
The traditional view of central nervous system function presumed that learning is the province of the brain. From this perspective, the spinal cord functions primarily as a conduit for incoming/outgoing neural impulses, capable of organizing simple reflexes but incapable of learning. Research has challenged this view, demonstrating that neurons within the spinal cord, isolated from the brain by means of a spinal cut (transection), can encode environmental relations and that this experience can have a lasting effect on function. The exploration of this issue has been informed by work in the learning literature that establishes the behavioral criteria and work within the pain literature that has shed light on the underlying neurobiological mechanisms. Studies have shown that spinal systems can exhibit single stimulus learning (habituation and sensitization) and are sensitive to both stimulus–stimulus (Pavlovian) and response–outcome (instrumental) relations. Regular environmental relations can both bring about an alteration in the performance of a spinally mediated response and impact the capacity to learn in future situations. The latter represents a form of behavioral metaplasticity. At the neurobiological level, neurons within the central gray matter of the spinal cord induce lasting alterations by engaging the NMDA receptor and signal pathways implicated in brain-dependent learning and memory. Of particular clinical importance, uncontrollable/unpredictable pain (nociceptive) input can induce a form of neural over-excitation within the dorsal horn (central sensitization) that impairs adaptive learning. Pain input after a contusion injury can increase tissue loss and undermines long-term recovery.
Angel Ariel Caputi
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.
Richard L. Doty
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.
Cynthia M. Harley and Mark K. Asplen
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.
Jeffrey R. Holt and Gwenaëlle S.G. Géléoc
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.
Cynthia F. Moss
Echolocating bats have evolved an active sensing system, which supports 3D perception of objects in the surroundings and permits spatial navigation in complete darkness. Echolocating animals produce high frequency sounds and use the arrival time, intensity, and frequency content of echo returns to determine the distance, direction, and features of objects in the environment. Over 1,000 species of bats echolocate with signals produced in their larynges. They use diverse sonar signal designs, operate in habitats ranging from tropical rain forest to desert, and forage for different foods, including insects, fruit, nectar, small vertebrates, and even blood. Specializations of the mammalian auditory system, coupled with high frequency hearing, enable spatial imaging by echolocation in bats. Specifically, populations of neurons in the bat central nervous system respond selectively to the direction and delay of sonar echoes. In addition, premotor neurons in the bat brain are implicated in the production of sonar calls, along with movement of the head and ears. Audio-motor circuits, within and across brain regions, lay the neural foundation for acoustic orientation by echolocation in bats.
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.
Eric S. Wohleb
Proper immune function is critical to maintain homeostasis, recognize and eliminate pathogens, and promote tissue repair. Primary and secondary immune organs receive input from the autonomic nervous system and immune cells express receptors for epinephrine, norepinephrine, and/or acetylcholine. Through direct signaling the autonomic nervous system controls immune function by altering immune cell development, initiating redistribution of immune cells throughout the body, and promoting molecular pathways that shift immune cell reactivity. This neuroimmune communication allows the autonomic nervous system to shape immune function based on physiological and psychological demands.
Penile erection is a part of the human male sexual response, involving desire, excitation (erection), orgasm (ejaculation), and resolution, and autonomic nerves are involved in all phases. Autonomic innervation of smooth-muscle cells of the erectile tissue is provided by the cavernous nerve. Motor and sensory innervation is derived from the pudendal nerves and their terminal branches, that is, the dorsal nerves of the penis, which carry impulses from receptors harbored in the penile skin, prepuce, and glans. Erection begins with an increased flow in the pudendal arteries and dilatation of the cavernous arteries and helicine arterioles in association with relaxation of the smooth muscles of the trabecular network, causing engorgement of blood in the corpora. This leads to compression of subtunical venules by the resistant tunica albuginea and erection. During detumescence these events are reversed.
Paul J. May, Anton Reiner, and Paul D. Gamlin
The functions of the eye are regulated by and dependent upon the autonomic nervous system. The parasympathetic nervous system controls constriction of the iris and accommodation of the lens via a pathway with preganglionic motor neurons in the Edinger-Westphal nucleus and postganglionic motor neurons in the ciliary ganglion. The parasympathetic nervous system regulates choroidal blood flow and the production of aqueous humor through a pathway with preganglionic motor neurons in the superior salivatory nucleus and postganglionic motor neurons in the pterygopalatine (sphenopalatine) ganglion. The sympathetic nervous system controls dilation of the iris and may modulate the outflow of aqueous humor from the eye. The sympathetic preganglionic motor neurons lie in the intermediolateral cell column at the first level of the thoracic cord, and the postganglionic motor neurons are found in the superior cervical ganglion.
The central pathways controlling different autonomic functions in the eye are found in a variety of locations within the central nervous system. The reflex response of the iris to changes in luminance levels begins with melanopsin-containing retinal ganglion cells in the retina that project to the olivary pretectal nucleus. This nucleus then projects upon the Edinger-Westphal preganglionic motoneurons. The dark response that produces maximal pupillary dilation involves the sympathetic pathways to the iris. Pupil size is also regulated by many other factors, but the pathways to the parasympathetic and sympathetic preganglionic motoneurons that underlie this are not well understood. Lens accommodation is controlled by premotor neurons located in the supraoculomotor area. These also regulate the pupil, and control vergence angle by modulating the activity of medial rectus, and presumably lateral rectus, motoneurons. Pathways from the frontal eye fields and cerebellum help regulate their activity. Blood flow in the choroid is regulated with respect to systemic blood pressure through pathways through the nucleus of the tractus solitarius. It is also regulated with respect to luminance levels, which likely involves the suprachiasmatic nucleus, which receives inputs from melanopsin-containing retinal ganglion cells, and other areas of the hypothalamus that project upon the parasympathetic preganglionic neurons of the superior salivatory nucleus that mediate choroidal vasodilation.
Thad E. Wilson and Kristen Metzler-Wilson
Thermoregulation is a key physiologic homeostatic process and is subdivided into autonomic, behavioral, and adaptive divisions. Autonomic thermoregulation is a neural process related to the sympathetic and parasympathetic nervous systems. Autonomic thermoregulation is controlled at the subcortical level to alter physiologic processes of heat production and loss to maintain internal temperature. Mammalian, including human, autonomic responses to acute heat or cold stresses are dependent on environmental conditions and species genotype and phenotype, but many similarities exist. Responses to an acute heat stress begin with the sensation of heat, leading to central processing of the information and sympathetic responses via end organs, which can include sweat glands, vasculature, and airway and cardiac tissues. Responses to an acute cold stress begin with the sensation of cold, which leads to central processing of the information and sympathetic responses via end organs, which can include skeletal and piloerector muscles, brown adipose tissue, vasculature, and cardiac tissue. These autonomic responses allow homeostasis of internal temperature to be maintained across a wide range of external temperatures for most mammals, including humans. At times, uncompensable thermal challenges occur that can be maintained for only limited periods of time before leading to pathophysiologic states of hyperthermia or hypothermia.
Natalia Duque-Wilckens and Brian C. Trainor
Aggressive behavior plays an essential role in survival and reproduction across animal species—it has been observed in insects, fish, reptiles, and mammals including humans. Even though specific aggressive behaviors are quite heterogeneous across species, many of the underlying mechanisms modulating aggression are highly conserved. For example, in a variety of species arginine vasopressin (AVP) and its homologue vasotocin in the hypothalamus, play an important role in regulating aggressive behaviorssuch as territorial and inter male aggression. Similarly in the medial amygdala, activation of a subpopulation of GABAergic neurons promotes aggression, while the prefrontal cortex exerts inhibitory control over aggressive behaviors. An important caveat in the aggression literature is that it is focused primarily on males, probably because in most species males are more aggressive than females. However, female aggression is also highly prevalent in many contexts, as it can affect access to resources such as mates, food, and offspring survival. Although it is likely that many underlying mechanisms are shared between sexes, there is sex specific variation in aggression, type, magnitude, and contexts, which suggests that there are important sex differences in how aggression is regulated. For example, while AVP acts to modulate aggression in both male and female hamsters, it increases male aggression but decreases female aggression. These differences can occur at the extent of neurotransmitter or hormones release, sensitivity (i.e., receptor expression), and/or molecular responses.
Paul E. Nachtigall
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.
Colin J. Saldanha
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.
Nicolas Dallière, Lindy Holden-Dye, James Dillon, Vincent O'Connor, and Robert J. Walker
The microscopic free-living nematode worm Caenorhabditis elegans was the first metazoan to have its genome sequenced and for many decades has served as a genetically tractable model for the investigation of neural mechanisms of behavioral plasticity. Many of its behaviors involve the detection of its food, bacteria, which are ingested and transported to the intestine by a muscular pharynx. The structure of the pharynx and the circuitry of the pharyngeal nervous system that regulates pharyngeal activity have been described in some detail. This has provided a platform for understanding how this simple organism finely tunes its feeding behavior in response to the changing availability and quality of its food, and in the context of its own nutritional status. This resonates with fundamental principles of energy homeostasis that occur throughout the animal kingdom.
James S.H. Wong and Catharine H. Rankin
The nematode, Caenorhabditis elegans (C. elegans), is an organism useful for the study of learning and memory at the molecular, cellular, neural circuitry, and behavioral levels. Its genetic tractability, transparency, connectome, and accessibility for in vivo cellular and molecular analyses are a few of the characteristics that make the organism such a powerful system for investigating mechanisms of learning and memory. It is able to learn and remember across many sensory modalities, including mechanosensation, chemosensation, thermosensation, oxygen sensing, and carbon dioxide sensing. C. elegans habituates to mechanosensory stimuli, and shows short-, intermediate-, and long-term memory, and context conditioning for mechanosensory habituation. The organism also displays chemotaxis to various chemicals, such as diacetyl and sodium chloride. This behavior is associated with several forms of learning, including state-dependent learning, classical conditioning, and aversive learning. C. elegans also shows thermotactic learning in which it learns to associate a particular temperature with the presence or absence of food. In addition, both oxygen preference and carbon dioxide avoidance in C. elegans can be altered by experience, indicating that they have memory for the oxygen or carbon dioxide environment they were reared in.
Many of the genes found to underlie learning and memory in C. elegans are homologous to genes involved in learning and memory in mammals; two examples are crh-1, which is the C. elegans homolog of the cAMP response element-binding protein (CREB), and glr-1, which encodes an AMPA glutamate receptor subunit. Both of these genes are involved in long-term memory for tap habituation, context conditioning in tap habituation, and chemosensory classical conditioning. C. elegans offers the advantage of having a very small nervous system (302 neurons), thus it is possible to understand what these conserved genes are doing at the level of single identified neurons. As many mechanisms of learning and memory in C. elegans appear to be similar in more complex organisms including humans, research with C. elegans aids our ever-growing understanding of the fundamental mechanisms of learning and memory across the animal kingdom.
Douglas K. Reilly and Jagan Srinivasan
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.
In response to changes in metabolic demand, the cardiovascular and respiratory systems are regulated in a highly coordinated fashion, such that both ventilation and cardiac output increase in a parallel fashion, thus maintaining a relatively constant level of arterial blood PO2, PCO2, and pH. In addition, external alerting stimuli that trigger defensive or orienting behavioral responses also trigger coordinated cardiorespiratory changes that are appropriate for the particular behavior. Furthermore, environmental challenges such as hypoxia or submersion evoke complex cardiovascular and respiratory response that have the effect of increasing oxygen uptake and/or conserving the available oxygen.
The brain mechanisms that are responsible for generating coordinated cardiorespiratory responses can be divided into reflex mechanisms and feedforward (central command) mechanisms. Reflexes that regulate cardiorespiratory function arise from a wide variety of internal receptors, and include those that signal changes in blood pressure, the level of blood oxygenation, respiratory activity, and metabolic activity. In most cases more than one reflex is activated, so that the ultimate cardiorespiratory response depends upon the interaction between different reflexes. The essential central pathways that subserve these reflexes are largely located within the brainstem and spinal cord, although they can be powerfully modulated by descending inputs arising from higher levels of the brain. The brain defense mechanisms that regulate the cardiorespiratory responses to external threatening stimuli (e.g., the sight, sound, or odor of a predator) are highly complex, and include both subcortical and cortical systems. The subcortical system, which includes the basal ganglia and midbrain colliculi as essential components, is phylogenetically ancient and generates immediate coordinated cardiorespiratory and motor responses to external stimuli. In contrast, the defense system that includes the cortex, hypothalamus, and limbic system evolved at a later time, and is better adapted to generating coordinated responses to external stimuli that involve cognitive appraisal.
Simona Candiani and Mario Pestarino
The central and peripheral nervous systems of amphioxus adults and larvae are characterized by morphofunctional features relevant to understanding the origins and evolutionary history of the vertebrate CNS. Classical neuroanatomical studies are mainly on adult amphioxus, but there has been a recent focus, both by TEM and molecular methods, on the larval CNS. The latter is small and remarkably simple, and new data on the localization of glutamatergic, GABAergic/glycinergic, cholinergic, dopaminergic, and serotonergic neurons within the larval CNS are now available. In consequence, it has been possible begin the process of identifying specific neuronal circuits, including those involved in controlling larval locomotion. This is especially useful for the insights it provides into the organization of comparable circuits in the midbrain and hindbrain of vertebrates. A much better understanding of basic chordate CNS organization will eventually be possible when further experimental data will emerge.
Z. Yan Wang and Clifton W. Ragsdale
Over 700 species of cephalopods live in the Earth’s waters, occupying almost every marine zone, from the benthic deep to the open ocean to tidal waters. The greatly varied forms and charismatic behaviors of these animals have long fascinated humans. Cephalopods are short-lived, highly mobile predators with sophisticated brains that are the largest among the invertebrates. While cephalopod brains share a similar anatomical organization, the nervous systems of coleoids (octopus, squid, cuttlefish) and nautiloids all display important lineage-specific neural adaptations. The octopus brain, for example, has for its arms a well-developed tactile learning and memory system that is vestigial in, or absent from, that of other cephalopods. The unique anatomy of the squid giant fiber system enables rapid escape in the event of capture. The brain of the nautilus comprises fewer lobes than its coleoid counterparts, but contains olfactory system structures and circuits not yet identified in other cephalopods.