John C. Montgomery

Structure and function of the vertebrate magnetic sense

Some vertebrates can navigate over long distances using the Earths magnetic field, but the sensory system that they use to do so has remained a mystery. Here we describe the key components of a magnetic sense underpinning this navigational ability in a single species, the rainbow trout ( Oncorhynchus mykiss). We report behavioural and electrophysiological responses to magnetic fields and identify an area in the nose of the trout where candidate magnetoreceptor cells are located. We have tracked the sensory pathway from these newly identified candidate magnetoreceptor cells to the brain and associated the system with a learned response to magnetic fields.

The lateral line can mediate rheotaxis in fish

Rheotaxis is a behavioural orientation to water currents. It has been demonstrated physiologically that some lateral-line receptors are particularly well suited to provide information on water currents, but their contribution to rheotaxis has been largely overlooked. The accepted view is that rheotaxis is mediated by visual and tactile cues, and that in rheotactic orientation “the lateral lines play only a minor role”. Here we provide a direct demonstration that rheotaxis can be mediated by the lateral line, and indeed by one specific receptor class of this system. In three diverse fish species, pharmacological block of the entire lateral-line system substantially increases the velocity threshold for rheotactic behaviour. The same effect is observed when only superficial neuromasts are ablated, whereas blockade of the other receptor class, canal neuromasts, has no such effect. Our results therefore demonstrate that superficial neuromasts make an important contribution to rheotactic behaviour in fish.

The Generation and Subtraction of Sensory Expectations within Cerebellum-Like Structures

The generation of expectations about sensory input and the subtraction of such expectations from actual input appear to be important features of sensory processing. This paper describes the generation of sensory expectations within cerebellum-like structures of four distinct groups of fishes: Mormyridae; Rajidae; Scorpaenidae; and Apteronotidae. These structures consist of a sheet-like array of principal cells. Apical dendrites of the principal cells extend out into a molecular layer where they are contacted by parallel fibers. The basilar regions of the arrays receive primary afferent input from octavolateral endorgans, i.e., electroreceptors, mechanical lateral line neuromasts, or eighth nerve endorgans. The parallel fibers in the molecular layer convey various types of information, including corollary discharge signals associated with motor commands, sensory information from other modalities such as proprioception, and descending input from higher stages of the sensory modality that is processed by the structure. Associations between the signals conveyed by the parallel fibers and particular patterns of sensory input to the basal layers lead to the generation of a negative image of expected sensory input within the principal cell array. Addition of this negative image to actual sensory input results in the subtraction of expected from actual input, allowing the unexpected or novel input to stand out more clearly. Intracellular recording indicates that the negative image is probably generated by means of anti-Hebbian synaptic plasticity at the parallel fiber to principal cell synapse. The results are remarkably similar in the different fishes and may generalize to cerebellum-like structures in other sensory systems and taxa.

Sound as an Orientation Cue for the Pelagic Larvae of Reef Fishes and Decapod Crustaceans

The pelagic life history phase of reef fishes and decapod crustaceans is complex, and the evolutionary drivers and ecological consequences of this life history strategy remain largely speculative. There is no doubt, however, that this life history phase is very significant in the demographics of reef populations. Here, we initially discuss the ecology and evolution of the pelagic life histories as a context to our review of the role of acoustics in the latter part of the pelagic phase as the larvae transit back onto a reef. Evidence is reviewed showing that larvae are actively involved in this transition. They are capable swimmers and can locate reefs from hundreds of metres if not kilometres away. Evidence also shows that sound is available as an orientation cue, and that fishes and crustaceans hear sound and orient to sound in a manner that is consistent with their use of sound to guide settlement onto reefs. Comparing particle motion sound strengths in the field (8 x 10(-11) m at 5 km from a reef) with the measured behavioural and electrophysiological threshold of fishes of (3 x 10(-11) m and 10 x 10(-11), respectively) provides evidence that sound may be a useful orientation cue at a range of kilometres rather than hundreds of metres. These threshold levels are for adult fishes and we conclude that better data are needed for larval fishes and crustaceans at the time of settlement. Measurements of field strengths in the region of reefs and threshold levels are suitable for showing that sound could be used; however, field experiments are the only effective tool to demonstrate the actual use of underwater sound for orientation purposes. A diverse series of field experiments including light-trap catches enhanced by replayed reef sound, in situ observations of behaviour and sound-enhanced settlement rate on patch reefs collectively provide a compelling case that sound is used as an orientation and settlement cue for these late larval stages.

The Enigmatic Lateral Line System

Hearing in its broadest sense is the detection, by specialized mechanoreceptors, of mechanical energy propagated through the environment. In terrestrial vertebrates, this typically means inner ear transduction of air pressure waves radiating out from a sound source, though the detection of substrate vibrations can also be considered as a form of hearing. In aquatic environments, the extended contribution of incompressible flow in the near field of the source adds additional complexities, and both incompressible flow and propagated pressure waves are detected by a range of specialized hair cell mechanosensory systems. Hair cells are generalized mechanical transducers that respond to mechanical deformation of the receptor hairs at their apical surface. One of the interesting stories of hearing in general, and in aquatic vertebrates in particular, is how the structures associated with hair cell organs play a major role in modifying or channeling the environmental stimulus onto the hair cell receptors. Hence the peripheral anatomy determines to a large degree what particular stimulus feature is being encoded at the level of the hair cell.

An adaptive filter that cancels self-induced noise in the electrosensory and lateral line mechanosensory systems of fish ☆

In lateral line and electrosensory systems of fish, the animals own movements create unwanted stimulation that could interfere with the detection of biologically important signals. Here we report that an adaptive filter in the medullary nuclei of both senses suppresses self-stimulation. Second-order electrosensory neurons in an elasmobranch fish and mechanosensory neurons in a teleost fish learn to cancel the effects of stimuli that are presented coupled to the fishs movements. A model is proposed for how the adaptive filter is realized by the cerebellar-like circuits of the hindbrain nuclei in these senses.

Comparative physiology of Antarctic fishes

Publisher Summary From the standpoint of a comparative physiologist, Antarctica is a superb natural laboratory providing excellent research opportunities. The unique fish fauna of an entire continent has resulted from the successful colonization of Antarctic waters, and subsequent diversification, by a single major group. The results of these studies on the comparative physiology of Antarctic fishes have implications for a wide range of biological disciplines. The complex of physiological adaptations of notothenioid fishes gives some insight into the reasons for their success as the major group of Antarctic teleosts, and the general failure of other fishes to penetrate south of the Antarctic Convergence. The attempts to understand the effects of temperature on biological processes, and its consequences for the animals themselves, will always be highlighted by the study of extreme environments. This chapter summarizes the progress in Antarctic fish physiology made over the past quarter century, to indicate the exciting potential for further work, and to act as an introduction to new workers in the field.

The Mechanosensory Lateral Line System of the Hypogean form of Astyanax Fasciatus

The mechanosensory lateral line is a distributed, hair-cell based system which detects the water flow regime at the surface of the fish. Superficial neuromasts densely scattered over the surface of some cave fish detect the pattern of flow over the surface of the body and are important in rheotactic behaviors and perhaps in the localization of small vibrating sources. Canal neuromasts are very likely also involved in the detection of small planktonic prey, but seem also to play an essential role in replacing vision as the major sense by which blind cave-fish perceive their surroundings. The flow-field that exists around a gliding fish is perturbed by objects in the immediate vicinity, these perturbations are detected by the lateral line system. In this way the fish can build up a ‘picture’ of its environment, a process that has been called active hydrodynamic imaging. None of the lateral line behaviors exhibited by blind cave fish are necessarily exclusive to these species, but there is some evidence that their lateral line capabilities are enhanced with respect to their sighted relatives.

The sensory basis of rheotaxis in the blind Mexican cave fish, Astyanax fasciatus

Abstract The sensory basis of rheotaxis (orientation to currents) was investigated in the blind Mexican cave fish, Astyanax fasciatus. An unconditioned rheotactic response to uniform velocity flows was exhibited, with a threshold of less than 3 cm s−1. Disabling the entire lateral line or the superficial neuromast receptor class increased the rheotactic threshold to greater than 9 cm s−1. A pharmacological block of the lateral line canal system alone had no effect. These results demonstrate that the superficial lateral line system controls rheotaxis at low current velocities. The effect of pairing an odor stimulant with the water current dropped the rheotactic threshold to less than 0.4 cm s−1. This study provides a clear behavioral role for the superficial neuromasts where none previously existed, and also establishes a link between the mechanosensory lateral line and olfactory systems in the olfactory search behavior of the cave fish.

Variation in brain organization and cerebellar foliation in chondrichthyans: Sharks and holocephalans

The widespread variation in brain size and complexity that is evident in sharks and holocephalans is related to both phylogeny and ecology. Relative brain size (expressed as encephalization quotients) and the relative development of the five major brain areas (the telencephalon, diencephalon, mesencephalon, cerebellum, and medulla) was assessed for over 40 species from 20 families that represent a range of different lifestyles and occupy a number of habitats. In addition, an index (1–5) quantifying structural complexity of the cerebellum was created based on length, number, and depth of folds. Although the variation in brain size, morphology, and complexity is due in part to phylogeny, as basal groups have smaller brains, less structural hypertrophy, and lower foliation indices, there is also substantial variation within and across clades that does not reflect phylogenetic relationships. Ecological correlations, with the relative development of different brain areas as well as the complexity of the cerebellar corpus, are supported by cluster analysis and are suggestive of a range of ‘cerebrotypes’. These correlations suggest that relative brain development reflects the dimensionality of the environment and/or agile prey capture in addition to phylogeny.