Christopher B. Braun

What Is the Nature of Multisensory Interaction between Octavolateralis Sub-Systems?

The octavolateralis system consists of several submodalities, including the inertial-sensitive inner ear, the pressure-sensitive ear/air cavity complex (when present), and acceleration- and velocity-sensitive components of the lateral line system (canal and superficial neuromasts, respectively). All four of these channels are responsive to many of the same stimulus sources, particularly moving or vibrating objects within a short distance from the receiver. We therefore argue that the octavolateralis system is an excellent model for the study of multisensory interactions. We focus on the possible ways in which these channels may contribute to source localization mechanisms and to the multisensory guidance of behaviors with strong directional components (e.g., predator avoidance, prey capture and mate attraction). Finally, we define four ways in which information from multiple senses might interact. These include fractionation, synergy, accessory stimulation, and complementation. Although evidence for all types of octavolateralis interactions can be found, the primary modes of interaction appear to be complementation and fractionation. For example, the inertial and pressure-sensitive submodalities of the auditory system provide complementary pieces of information about the direction (e.g., left/right) and polarity (advancing or receding) of a moving source. In contrast, the lateral line canal system subserves short-range localization tasks, whereas the auditory system may subserve longer-range detection and localization tasks.

The Sensory Biology of the Living Jawless Fishes: A Phylogenetic Assessment

Despite the ancient origins and aberrant appearance of living jawless fishes, none of their features may be assumed to be primitive without comparisons among hagfishes, lampreys, and gnathostomes, and with the nearest relatives of all craniates, the cephalochordates. In this review, the sensory capabilities of lampreys and hagfishes will be compared, and the major features of early craniate sensory evolution will be infered using cladistic methodology and an accepted phylogeny of the hagfishes, lampreys and gnathostomes. Lampreys have well developed olfactory, visual and octavolateralis systems, each of which is known to play a role in lamprey life and behavior. Hagfishes have poorly developed visual and octavolateralis systems, but elaborate olfactory and chemosensory systems. Unfortunately, the natural behavior and lifestyle of hagfishes are poorly known, limiting our understanding of hagfish sensory biology. Both groups of living jawless fishes show mixtures of primitive and secondarily derived sensory features and have few shared derived sensory features that would indicate close relations between the two groups.

Evolution of Peripheral Mechanisms for the Enhancement of Sound Reception

The evolutionary history of hearing is a rich and fascinating pageant. The inner ear and the closely related mechanosensory lateral line show a tremendous diversity among living and fossil vertebrates. This chapter documents how these systems have evolved new functions by juxtaposing novel linkages (i.e., transduction mechanisms) between fundamentally conservative hair cell sensors and the outside world. These linkages dictate the ear’s function, and are so diverse that the functions of the ear (and lateral line) have changed repeatedly in vertebrate history. The linkages of the vertebrate ear do indeed bring joy to the comparative biologist, and the evolution of these linkages is the evolution of new sensory functions, many of which may have led to the rapid diversification of individual taxa (e.g., Otophysi) and the expansion of behavioral repertoires. To discuss the evolution of enhanced hearing capabilities, one must understand the primitive functions of the octavolateralis systems, and ask what new functions has evolution wrought, and what are the new stimuli to which the ear responds in derived taxa? To constrain the discussion of the diversity of inner ear linkages, this chapter reviews the evolution of specializations that alter the function of the inner ear in teleost fishes and grant the ability to detect fluctuations in the ambient pressure (i.e., sound). Several instances of lateral line specialization that may provide this system with pressure sensitivity are also described. When the distribution of these specializations is compared to our best estimates of teleost relationships (Fig. 4.1), it appears that the detection of pressure fluctuations (what terrestrially chauvinistic vertebrates call hearing) has evolved dozens of times! This chapter describes some of these novel morphologies in detail and attempts

Information Processing by the Lateral Line System

This review covers four areas of research that have fruitfully contributed to our understanding of lateral line function within the past 10 years. One striking aspect of the lateral line system is its tremendous diversity. Recent findings, however, indicate a functional constancy that may be maintained by relatively subtle morphological features. Other morphological variations have been shown to enhance sensitivity at particular frequency bandwidths. A second area of research has focused on hydrodynamic imaging and the peripheral patterns of receptor excitation that might encode stimulus features such as amplitude, distance, location, and direction of motion. A detailed model is described and provides several predictions for the types of information passed from the periphery to the central nervous system (CNS).The third topic covered is the mechanisms that enhance signal detection in noisy backgrounds. It is becoming clear that canals act as biomechanical filters to improve signal-to-noise ratios in the presence of lowfrequency noises such as uniform, ambient water motions. Two central mechanisms, efferent modulation of receptor excitation and a central dynamic filter mechanism, have been shown to reduce reafference due to self-generated noise and may enhance signal detection in general. The second central mechanism is postulated to be similar to the anti-hebbian learning mechanism that has been well documented within the related electrosensory system. Finally, this review covers the recently documented roles of the lateral line system in natural behaviors, including courtship and prey capture. Some of these recent studies have led to the exciting conclusion that the lateral line may be composed of two distinct information channels, one served by canal and the other by superficial neuromasts, and that each may be dedicated to different behavioral tasks.

Schreiner organs: A new craniate chemosensory modality in hagfishes

An extensive system of sensory organs resembling taste buds was previously known in the skin of hagfishes. These sensory organs, called here Schreiner organs, are found throughout the epidermis of both Eptatretus stoutii and Myxine glutinosa. They are found also at high densities in the prenasal sinus, nasopharyngeal duct, and pharynx, and at lower densities in the oral and velar chambers. Schreiner organs are multicellular aggregates composed of acetylated tubulin‐immunoreactive receptor cells and nonimmunoreactive cells. A considerable range of variation was found in Schreiner organ morphology, but discrete classes of organs could not be recognized. Schreiner organs are innervated by all sensory trigeminal rami, the glossopharyngeal/vagal nerve, and cutaneous rami of spinal nerves, but not by the facial nerve. The central projections of these rami form a continuous tract in the trigeminal sensory zone and the dorsolateral funiculus of the spinal cord. Some Schreiner organs may be represented in the nucleus of the solitary tract, but this structure is certainly not the primary recipient zone of Schreiner organ afferents. In light of these systemic differences between vertebrate taste systems and the Schreiner organ system of hagfishes, it is concluded that Schreiner organs are not homologous to taste buds. This sensory modality of hagfishes has no direct homolog in vertebrates and appears to be a specialization of hagfishes, perhaps derived from the primitive somatosensory system of the earliest craniates. J. Comp. Neurol. 392:135–163, 1998.

Cutaneous Exteroreceptors and their Innervation in Hagfishes

Earlier portrayals of hagfish biology and behaviour are inconsistent with emerging evidence of hagfish sensory capabilities and ecology. Hagfishes may be characterized as chemosensory specialists, perhaps actively preying on invertebrates in the benthic and endobenthic habitat. Two sensory systems are examined in detail: the lateral line system and a chemoreceptive system which is unique to hagfishes. The lateral line system is composed of a small number of sensory patches with a simpler organization than the neuromasts of vertebrate lateral line systems. The simplicity of eptatretid lateral line systems is argued to be derived via regressive evolution in relation to burrowing habits. Potentially primitive features of the lateral line system of hagfish may be limited to the morphology of the receptor cells themselves. This simplicity and apparently paltry sensory capability is contrasted with an elaborate cutaneous chemosensory system: the Schreiner organ system. Schreiner organs are compound organs of sensory and support cells whose cytology resembles similar cell types in vertebrate taste buds. Schreiner organs are distributed quite densely on the tentacles, snout, prenasal sinus and nasopharyngeal duct, and at more modest densities in the pharynx and the epidermis of the head, trunk and tail. Schreiner organs are innervated by branches of the trigeminal, vagal and spinal nerves. This advanced sensory system rivals the most elaborate gustatory systems of vertebrates (e.g. siluriform teleosts) and is interpreted as a convergent adaptation to a dark and turbid habitat. Analysis of both the lateral line and Schreiner organ systems indicates that the sensory world of hagfishes is far richer than previously assumed.

Distribution and Innervation of Taste Buds in the Axolotl

Adult axolotls have approximately 1,400 taste buds in the epithelium of the pharyngeal roof and floor and the medial surfaces of the visceral bars. These receptors are most dense on the lingual surfaces of the upper and lower jaws, slightly less dense throughout lateral portions of the pharyngeal roof and floor, and more sparse within medial portions of the pharyngeal roof and floor, except for a median oval patch of receptors located rostrally between the vomerine tooth fields. Each taste bud is a pear-shaped organ, situated at the center of a raised hillock and averaging 80 and 87 µm in height and width, respectively. Each comprises 50 to 80 cells, which can be classified as basal, dark fusiform, or light fusiform, based on differences in their morphology. The distal ends of the apical processes of the fusiform cells reach the surface of each hillock, forming a single taste pore with an average diameter of 15 µm. Each apical process terminates in one of three ways: as short, evenly spaced microvilli; as long clustered microvilli; or as large, stereocilia-like microvilli. The pharyngeal epithelium and associated taste buds in axolotls are innervated solely by rami of the facial, glossopharyngeal and vagal nerves. Approximately, the rostral one half of the pharyngeal roof is innervated by the palatine rami of the facial nerve, whereas the caudal one half of the pharyngeal roof is innervated by the pharyngeal rami of the glossopharyngeal and vagal nerves. The lingual surface of the lower jaw is innervated by the pretrematic (mandibular) ramus of the facial nerve. The dorsal two-thirds of the visceral arches, and the ventral one-third of the visceral arches and the pharyngeal floor, are innervated by both the pretrematic and post-trematic rami of the glossopharyngeal and vagal nerves, respectively.

The hydrodynamic footprint of a benthic, sedentary fish in unidirectional flow.

Mottled sculpin (Cottus bairdi) are small, benthic fish that avoid being swept downstream by orienting their bodies upstream and extending their large pectoral fins laterally to generate negative lift. Digital particle image velocimetry was used to determine the effects of these behaviors on the spatial and temporal characteristics of the near-body flow field as a function of current velocity. Flow around the fishs head was typical for that around the leading end of a rigid body. Flow separated around the edges of pectoral fin, forming a wake similar to that observed for a flat plate perpendicular to the flow. A recirculation region formed behind the pectoral fin and extended caudally along the trunk to the approximate position of the caudal peduncle. In this region, the time-averaged velocity was approximately one order of magnitude lower than that in the freestream region and flow direction varied over time, resembling the periodic shedding of vortices from the edge of a flat plate. These results show that the mottled sculpin pectoral fin significantly alters the ambient flow noise in the vicinity of trunk lateral line sensors, while simultaneously creating a hydrodynamic footprint of the fishs presence that may be detected by the lateral line of nearby fish.

EVOLUTION OF THE WEBERIAN APPARATUS

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The temporal resolution of goldfish hearing: An auditory evoked potential study of gap detection

Temporal processing in goldfish (Carassius auratus) was studied by measuring auditory evoked potentials (AEP) using gaps in continuous band‐limited Gaussian noise. Long (>100 ms) silent gaps in high amplitude noise (30 dB SL) evoked distinct offset and onset responses, lasting 6090 ms. Offset and onset responses overlapped with shorter gaps and became difficult to distinguish for gaps <10 ms. The gap‐response waveform was modeled as the sum of offset and temporally‐shifted onset responses from the same animals (using 120‐ms gaps). This model predicted the waveform of gap responses nearly perfectly for gaps longer than 6 ms. Waveforms evoked by shorter gaps (<6 ms) did not accurately fit this model, suggesting that one or both components of the gap response were inhibited or altered. Nonetheless, clear responses were evoked by gaps shorter than 1 ms at this intensity, while longer gaps (up to 10 ms) were required for detection in a low‐intensity noise background. This study extends and confirms prior repor...