Roles for cerebellum and subsumption architecture in central pattern generation.

Within vertebrates, central pattern generators drive rhythmical behaviours, such as locomotion and ventilation. Their pattern generation is also influenced by sensory input and various forms of neuromodulation. These capabilities arose early in vertebrate evolution, preceding the evolution of the cerebellum in jawed vertebrates. This later evolution of the cerebellum is suggestive of subsumption architecture that adds functionality to a pre-existing network. From a central-pattern-generator perspective, what additional functionality might the cerebellum provide? The suggestion is that the adaptive filter capabilities of the cerebellum may be able to use error learning to appropriately repurpose pattern output. Examples may include head and eye stabilization during locomotion, song learning, and context-dependent alternation between learnt motor-control sequences.

Comparison of acoustic particle acceleration detection capabilities in three shark species.

Behavioural studies have shown that sharks are capable of directional orientation to sound. However, only one previous experiment addresses the physiological mechanisms of directional hearing in sharks. Here, we used a directional shaker table in combination with the auditory evoked potential (AEP) technique to understand the broadscale directional hearing capabilities in the New Zealand carpet shark (Cephaloscyllium isabellum), rig shark (Mustelus lenticulatus) and school shark (Galeorhinus galeus). The aim of this experiment was to test if sharks are more sensitive to vertical (z-axis) or head-to-tail (x-axis) accelerations, and whether there are any differences between species. Our results support previous findings, suggesting that shark ears can receive sounds from all directions. Acceleration detection bandwidth was narrowest for the carpet shark (40-200 Hz), and broader for rig and school sharks (40-800 Hz). Greatest sensitivity bands were 40-80 Hz for the carpet shark, 100-200 Hz for the rig and 80-100 Hz for the school shark. Our results indicate that there may be differences in directional hearing abilities among sharks. The bottom-dwelling carpet shark was equally sensitive to vertical and head-to-tail particle accelerations. In contrast, both benthopelagic rig and school sharks appeared to be more sensitive to vertical accelerations at frequencies up to 200 Hz. This is the first study to provide physiological evidence that sharks may differ in their directional hearing and sound localisation abilities. Further comparative physiological and behavioural studies in more species with different lifestyles, habitats and feeding strategies are needed to further explore the drivers for increased sensitivity to vertical accelerations among elasmobranchs.

Comparison of auditory evoked potential thresholds in three shark species.

Auditory sensitivity measurements have been published for only 12 of the more than 1150 extant species of elasmobranchs (sharks, skates and rays). Thus, there is a need to further understand sound perception in more species from different ecological niches. In this study, the auditory evoked potential (AEP) technique was used to compare hearing abilities of the bottom-dwelling New Zealand carpet shark (Cephaloscyllium isabellum) and two benthopelagic houndsharks (Triakidae), the rig (Mustelus lenticulatus) and the school shark (Galeorhinus galeus). AEPs were measured in response to tone bursts (frequencies: 80, 100, 150, 200, 300, 450, 600, 800 and 1200 Hz) from an underwater speaker positioned 55 cm in front of the shark in an experimental tank. AEP detection thresholds were derived visually and statistically, with statistical measures slightly more sensitive (∼4 dB) than visual methodology. Hearing abilities differed between species, mainly with respect to bandwidth rather than sensitivity. Hearing was least developed in the benthic C. isabellum [upper limit: 300 Hz, highest sensitivity: 100 Hz (82.3±1.5 dB re. 1 µm s-2)] and had a wider range in the benthopelagic rig and school sharks [upper limit: 800 Hz; highest sensitivity: 100 Hz (79.2±1.6 dB re. 1 µm s-2) for G. galeus and 150 Hz (74.8±1.8 dB re. 1 µm s-2) for M. lenticulatus]. The data are consistent with those known for 'hearing non-specialist' teleost fishes that detect only particle motion, not pressure. Furthermore, our results provide evidence that benthopelagic sharks exploit higher frequencies (max. 800 Hz) than some of the bottom-dwelling sharks (max. 300 Hz). Further behavioural and morphological studies are needed to identify what ecological factors drive differences in upper frequency limits of hearing in elasmobranchs.

Fish bioacoustics: Navigating underwater sound.

Fish bioacoustics is about the sounds produced by fish, how fish hear, and what they hear. The focus of this article is on the hypothesis that some late pelagic stage reef fish larvae use the marine soundscape to locate reef settlement habitat. The hypothesis is evaluated by consideration of the nature of reef sound, hearing ability in late-stage larval fish, and direct behavioral evidence for orientation to reef sound.

The use of evoked potentials to determine sensory sub-modality contributions to acoustic and hydrodynamic sensing.

Both the lateral line and the inner ear contribute to near-field dipole source detection in fish. The precise roles these two sensory modalities provide in extracting information about the flow field remain of interest. In this study, evoked potentials (EP, 30-200 Hz) for blind Mexican cavefish were measured in response to a dipole source. Greatest sensitivity was observed at the lower and upper ends of the tested frequency range. To evaluate the relative contributions of the lateral line and inner ear, we measured the effects of neomycin on EP response characteristics at 40 Hz, and used the vital dye DASPEI to verify neuromast ablation. Neomycin increased the latency of the EP response up until 60 min post-treatment. DASPEI results confirmed that neuromast hair cell death was significant in treated fish over this timeframe. These results indicate that the inner ear, whether it is sound pressure or particle motion detection, makes a significant contribution to the dipole-induced EP in blind cavefish at near-field low frequencies where the lateral line contribution would be expected to be strongest. The results from this study imply that under some circumstances, lateral line function could be complemented by the inner ear.

Ecology of fish hearing.

Underwater sound is directional and can convey important information about the surrounding environment or the animal emitting the sound. Therefore, sound is a major sensory channel for fishes and plays a key role in many life-history strategies. The effect of anthropogenic noise on aquatic life, which may be causing homogenisation or fragmentation of biologically important signals underwater is of growing concern. In this review we discuss the role sound plays in the ecology of fishes, basic anatomical and physiological adaptations for sound reception and production, the effects of anthropogenic noise and how fishes may be coping to changes in their environment, to put the ecology of fish hearing into the context of the modern underwater soundscape.

Marine bioacoustics.

The marine environment is the planet's largest, yet in many respects the least accessible. Our human sensory repertoire, with its emphasis on vision and air-adapted hearing, does not serve us well underwater. Underwater vision is often limited and as divers we find hearing of little, or no, use. Yet we know from the physics that underwater sound has properties well suited to serve as sensory and communication channels for suitably-adapted marine animals. The rapidly developing area of marine bioacoustics seeks to characterise underwater sound in relation to the acoustic capability of particular species (acoustic habitat), and discover the role of acoustics in the lives of marine animals (acoustic ecology) (Clarke et al., 2011).

Vocalisation Repertoire of Female Bluefin Gurnard (Chelidonichthys kumu) in Captivity: Sound Structure, Context and Vocal Activity.

Fish vocalisation is often a major component of underwater soundscapes. Therefore, interpretation of these soundscapes requires an understanding of the vocalisation characteristics of common soniferous fish species. This study of captive female bluefin gurnard, Chelidonichthys kumu, aims to formally characterise their vocalisation sounds and daily pattern of sound production. Four types of sound were produced and characterised, twice as many as previously reported in this species. These sounds fit two aural categories; grunt and growl, the mean peak frequencies for which ranged between 129 to 215 Hz. This species vocalized throughout the 24 hour period at an average rate of (18.5 ± 2.0 sounds fish-1 h-1) with an increase in vocalization rate at dawn and dusk. Competitive feeding did not elevate vocalisation as has been found in other gurnard species. Bluefin gurnard are common in coastal waters of New Zealand, Australia and Japan and, given their vocalization rate, are likely to be significant contributors to ambient underwater soundscape in these areas.

Vocalisations of the bigeye Pempheris adspersa: characteristics, source level and active space.

Fish sounds are an important biological component of the underwater soundscape. Understanding species-specific sounds and their associated behaviour is critical for determining how animals use the biological component of the soundscape. Using both field and laboratory experiments, we describe the sound production of a nocturnal planktivore, Pempheris adspersa (New Zealand bigeye), and provide calculations for the potential effective distance of the sound for intraspecific communication. Bigeye vocalisations recorded in the field were confirmed as such by tank recordings. They can be described as popping sounds, with individual pops of short duration (7.9±0.3 ms) and a peak frequency of 405±12 Hz. Sound production varied during a 24 h period, with peak vocalisation activity occurring during the night, when the fish are most active. The source level of the bigeye vocalisation was 115.8±0.2 dB re. 1 µPa at 1 m, which is relatively quiet compared with other soniferous fish. Effective calling range, or active space, depended on both season and lunar phase, with a maximum calling distance of 31.6 m and a minimum of 0.6 m. The bigeyes' nocturnal behaviour, characteristics of their vocalisation, source level and the spatial scale of its active space reported in the current study demonstrate the potential for fish vocalisations to function effectively as contact calls for maintaining school cohesion in darkness.

The cerebellum and cerebellum-like structures of cartilaginous fishes.

The cerebellum is well developed in cartilaginous fishes, with the same cell types (barring basket cells) and organizational features found in other vertebrate groups, including mammals. In particular, the lattice-like organization of cerebellar cortex (with a molecular layer of parallel fibers, interneurons, spiny Purkinje cell dendrites, and climbing fibers) is a defining characteristic. In addition to the cerebellum, cartilaginous fishes have cerebellum-like structures in the dorsolateral wall of the hindbrain. These structures are adjacent to and, in part, contiguous with the cerebellum. They are cerebellum-like in that they have a molecular layer of parallel fibers and inhibitory interneurons that has striking organizational similarities to the molecular layer of the cerebellar cortex. However, these structures also have characteristics that differ from the cerebellum. For example, cerebellum-like structures do not have climbing fibers and are clearly sensory. They receive direct afferent input from peripheral sensory receptors and relay their outputs to midbrain sensory areas. As a consequence of this close sensory association and the ability of researchers to characterize signal processing in these structures in a behaviorally relevant context, good progress has been made in determining the fundamental processing algorithm of the cerebellum-like structures. This algorithm enables the molecular layer to act as an adaptive filter that cancels self-generated noise in electrosensory and lateral line systems. Given the fundamental similarities of the molecular layer across these structures and the phylogeny of these structures across basal vertebrates, it is clear that these structures share a common genetic-developmental program. Syngeny is a term that has been used to describe similarity of structure due to a shared genetic-developmental program, whether the structures are phylogenetically homologous or not. Given that the cerebellum and cerebellum-like structures are physically adjacent, we propose that cerebellum-like structures were the evolutionary antecedent of the cerebellum and that the cerebellum arose through a change in the genetic-developmental program, amounting to a duplication of existing structure. Such duplication to form adjacent structures can be considered a special case of syngeny. On this view, the cerebellum is an evolutionary innovation in gnathostomes that is literally superimposed on pre-existing underlying brain structures and pathways. From this perspective, the cerebellum can be considered an example of 'subsumption architecture', a term that describes the addition of modules that add computational power while maintaining existing fundamental functionality. This addition is reflected in the finding that in elasmobranchs with relatively large brains, the size of the telencephalon and cerebellum enlarge disproportionately, while those parts of the brain that contain more direct sensory and motor connections do not. Added 'computational' power in the chondrichthyan brain and the comparative function and evolution of the cerebellum and cerebellum-like structures across the cartilaginous fishes supports the idea of the cerebellum as an example of subsumption architecture.

Disrupted flow sensing impairs hydrodynamic performance and increases the metabolic cost of swimming in the yellowtail kingfish, Seriola lalandi.

The yellowtail kingfish, Seriola lalandi, shows a distribution of anaerobic and aerobic (red and pink) muscle fibres along the trunk that is characteristic of active pelagic fishes. The athletic capacity of S. lalandi is also shown by its relative high standard metabolic rate and optimal (i.e. least cost) swimming speed. To test the hypothesis that lateral line afferent information contributes to efficient locomotion in an active pelagic species, the swimming performance of S. lalandi was evaluated after unilateral disruption of trunk superficial neuromasts (SNs). Unilaterally disrupting the SNs of the lateral line impaired both swimming performance and energetic efficiency. The critical swimming speed (U(crit); mean ± s.d., N=12) for unilaterally SN-disrupted fish was 2.11±0.96 fork lengths (FL) s(-1), which was significantly slower than the 3.66±0.19 FL s(-1) U(crit) of sham SN-disrupted fish. The oxygen consumption rate (mg O(2) kg(-1) min(-1)) of the unilaterally SN-disrupted fish in a speed range of 1.0-2.2 FL s(-1) was significantly greater than that of the sham SN-disrupted fish. The least gross cost of transport (GCOT; N=6) for SN-disrupted fish was 0.18±0.06 J N(-1) m(-1), which was significantly greater than the 0.11±0.03 J N(-1) m(-1) GCOT for sham SN-disrupted fish. The factorial metabolic scope (N=6) of the unilaterally SN-disrupted fish (2.87±0.78) was significantly less than that of sham controls (4.14±0.37). These data show that an intact lateral line is important to the swimming performance and efficiency of carangiform swimmers, but the functional mechanism of this effect remains to be determined.

Pressure and particle motion detection thresholds in fish: a re-examination of salient auditory cues in teleosts.

The auditory evoked potential technique has been used for the past 30 years to evaluate the hearing ability of fish. The resulting audiograms are typically presented in terms of sound pressure (dB re. 1 µPa) with the particle motion (dB re. 1 m s(-2)) component largely ignored until recently. When audiograms have been presented in terms of particle acceleration, one of two approaches has been used for stimulus characterisation: measuring the pressure gradient between two hydrophones or using accelerometers. With rare exceptions these values are presented from experiments using a speaker as the stimulus, thus making it impossible to truly separate the contribution of direct particle motion and pressure detection in the response. Here, we compared the particle acceleration and pressure auditory thresholds of three species of fish with differing hearing specialisations, goldfish (Carassius auratus, weberian ossicles), bigeye (Pempheris adspersus, ligamentous hearing specialisation) and a third species with no swim bladder, the common triplefin (Forstergyian lappillum), using three different methods of determining particle acceleration. In terms of particle acceleration, all three fish species have similar hearing thresholds, but when expressed as pressure thresholds goldfish are the most sensitive, followed by bigeye, with triplefin the least sensitive. It is suggested here that all fish have a similar ability to detect the particle motion component of the sound field and it is their ability to transduce the pressure component of the sound field to the inner ear via ancillary hearing structures that provides the differences in hearing ability. Therefore, care is needed in stimuli presentation and measurement when determining hearing ability of fish and when interpreting comparative hearing abilities between species.

Social aggregation in the pelagic zone with special reference to fish and invertebrates.

Aggregations of organisms, ranging from zooplankton to whales, are an extremely common phenomenon in the pelagic zone; perhaps the best known are fish schools. Social aggregation is a special category that refers to groups that self-organize and maintain cohesion to exploit benefits such as protection from predators, and location and capture of resources more effectively and with greater energy efficiency than could a solitary individual. In this review we explore general aggregation principles, with specific reference to pelagic organisms; describe a range of new technologies either designed for studying aggregations or that could potentially be exploited for this purpose; report on the insights gained from theoretical modelling; discuss the relationship between social aggregation and ocean management; and speculate on the impact of climate change. Examples of aggregation occur in all animal phyla. Among pelagic organisms, it is possible that repeated co-occurrence of stable pairs of individuals, which has been established for some schooling fish, is the likely precursor leading to networks of social interaction and more complex social behaviour. Social network analysis has added new insights into social behaviour and allows us to dissect aggregations and to examine how the constituent individuals interact with each other. This type of analysis is well advanced in pinnipeds and cetaceans, and work on fish is progressing. Detailed three-dimensional analysis of schools has proved to be difficult, especially at sea, but there has been some progress recently. The technological aids for studying social aggregation include video and acoustics, and have benefited from advances in digitization, miniaturization, motion analysis and computing power. New techniques permit three-dimensional tracking of thousands of individual animals within a single group which has allowed novel insights to within-group interactions. Approaches using theoretical modelling of aggregations have a long history but only recently have hypotheses been tested empirically. The lack of synchrony between models and empirical data, and lack of a common framework to schooling models have hitherto hampered progress; however, recent developments in this field offer considerable promise. Further, we speculate that climate change, already having effects on ecosystems, could have dramatic effects on aggregations through its influence on species composition by altering distribution ranges, migration patterns, vertical migration, and oceanic acidity. Because most major commercial fishing targets schooling species, these changes could have important consequences for the dependent businesses.

The flow fields involved in hydrodynamic imaging by blind Mexican cave fish (Astyanax fasciatus). Part I: open water and heading towards a wall.

Blind Mexican cave fish (Astyanax fasciatus) sense the presence of nearby objects by sensing changes in the water flow around their body. The information available to the fish using this hydrodynamic imaging ability depends on the properties of the flow field it generates while gliding and how this flow field is altered by the presence of objects. Here, we used particle image velocimetry to measure the flow fields around gliding blind cave fish as they moved through open water and when heading towards a wall. These measurements, combined with computational fluid dynamics models, were used to estimate the stimulus to the lateral line system of the fish. Our results showed that there was a high-pressure region around the nose of the fish, low-pressure regions corresponding to accelerated flow around the widest part of the body and a thick laminar boundary layer down the body. When approaching a wall head-on, the changes in the stimulus to the lateral line were confined to approximately the first 20% of the body. Assuming that the fish are sensitive to a certain relative change in lateral line stimuli, it was found that swimming at higher Reynolds numbers slightly decreased the distance at which the fish could detect a wall when approaching head-on, which is the opposite to what has previously been expected. However, when the effects of environmental noise are considered, swimming at higher speed may improve the signal to noise ratio of the stimulus to the lateral line.

The flow fields involved in hydrodynamic imaging by blind Mexican cave fish (Astyanax fasciatus). Part II: gliding parallel to a wall.

Blind Mexican cave fish (Astyanax fasciatus) are able to sense detailed information about objects by gliding alongside them and sensing changes in the flow field around their body using their lateral line sensory system. Hence the fish are able to build hydrodynamic images of their surroundings. This study measured the flow fields around blind cave fish using particle image velocimetry (PIV) as they swam parallel to a wall. Computational fluid dynamics models were also used to calculate the flow fields and the stimuli to the lateral line sensory system. Our results showed that characteristic changes in the form of the flow field occurred when the fish were within approximately 0.20 body lengths (BL) of a wall. The magnitude of these changes increased steadily as the distance between the fish and the wall was reduced. When the fish were within 0.02 BL of the wall there was a change in the form of the flow field owing to the merging of the boundary layers on the body of the fish and the wall. The stimuli to the lateral line appears to be sufficient for fish to detect walls when they are 0.10 BL away (the mean distance at which they normally swim from a wall), but insufficient for the fish to detect a wall when 0.25 BL away. This suggests that the nature of the flow fields surrounding the fish are such that hydrodynamic imaging can only be used by fish to detect surfaces at short range.

A conserved pattern of brain scaling from sharks to primates.

Several patterns of brain allometry previously observed in mammals have been found to hold for sharks and related taxa (chondrichthyans) as well. In each clade, the relative size of brain parts, with the notable exception of the olfactory bulbs, is highly predictable from the total brain size. Compared with total brain mass, each part scales with a characteristic slope, which is highest for the telencephalon and cerebellum. In addition, cerebellar foliation reflects both absolute and relative cerebellar size, in a manner analogous to mammalian cortical gyrification. This conserved pattern of brain scaling suggests that the fundamental brain plan that evolved in early vertebrates permits appropriate scaling in response to a range of factors, including phylogeny and ecology, where neural mass may be added and subtracted without compromising basic function.

Behavior and physiology of mechanoreception: separating signal and noise.

The mechanosensory lateral line is found in all aquatic fish and amphibians. It provides a highly sensitive and versatile hydrodynamic sense that is used in a wide range of behavior. Hydrodynamic stimuli of biological interest originate from both abiotic and biotic sources, and include water currents, turbulence and the water disturbances caused by other animals, such as prey, predators and conspecifics. However, the detection of biologically important stimuli often has to occur against a background of noise generated by water movement, or movement of the fish itself. As such, separating signal and noise is "of the essence" in understanding the behavior and physiology of mechanoreception. Here we discuss general issues of signal and noise in the lateral-line system and the behavioral and physiological strategies that are used by fish to enhance signal detection in a noisy environment. In order for signal and noise to be separated, they need to differ, and we will consider those differences under the headings of: frequency and temporal pattern; intensity discrimination; spatial separation; and mechanisms for the reduction of self-generated noise. We systematically cover the issues of signal and noise in lateral-line systems, but emphasize recent work on self-generated noise, and signal and noise issues related to prey search strategies and collision avoidance.

Variation in brain organization and cerebellar foliation in chondrichthyans: batoids.

Interspecific variation in relative brain size (encephalization), the relative size of the five major brain areas (the telencephalon, diencephalon, mesencephalon, cerebellum, and medulla) and the level of cerebellar foliation was assessed in over 20 representative species of batoid (skates and rays), from eight families. Using species as independent data points and phylogenetically independent contrasts, relationships among each of the neuroanatomical variables and two ecological variables, habitat and lifestyle, were assessed. Variation in relative brain size and brain organization appears to be strongly correlated with phylogeny. Members of the basal orders Rajiformes and Torpediniformes tend to have relatively small brains, with relatively small telencephalons, large medullas, and smooth, unfoliated cerebellums. More advanced Myliobatiformes possess relatively large brains, with relatively large telencephalons, small medullas, and complex, heavily foliated cerebellums. Increased brain size, telencephalon size, and cerebellar foliation also correlate with living in a complex habitat (such as in association with coral reefs) and an active, benthopelagic lifestyle, but as primary habitat and lifestyle also closely match phylogenetic relationships in batoids, it is difficult to separate the influence of phylogeny and ecological factors on brain organization in these animals. However, the results of two forms of multivariate analysis (principal component analysis and cluster analysis) reveal that certain species are clustered with others that share ecological traits, rather than with more closely related species from the same order. This suggests that ecological factors do play a role in defining patterns of brain organization and there is some evidence for 'cerebrotypes' in batoids.

Swimming kinematics and hydrodynamic imaging in the blind Mexican cave fish (Astyanax fasciatus).

Blind Mexican cave fish (Astyanax fasciatus) lack a functioning visual system, and are known to use self-generated water motion to sense their surroundings; an ability termed hydrodynamic imaging. Nearby objects distort the flow field created by the motion of the fish. These flow distortions are sensed by the mechanosensory lateral line. Here we used image processing to measure detailed kinematics, along with a new behavioural technique, to investigate the effectiveness of hydrodynamic imaging. In a head-on approach to a wall, fish reacted to avoid collision with the wall at an average distance of only 4.0+/-0.2 mm. Contrary to previous expectation, there was no significant correlation between the swimming velocity of the fish and the distance at which they reacted to the wall. Hydrodynamic imaging appeared to be most effective when the fish were gliding with their bodies held straight, with the proportion of approaches to the wall that resulted in collision increasing from 11% to 73% if the fish were beating their tails rather than gliding as they neared the wall. The swimming kinematics of the fish were significantly different when swimming beside a wall compared with when swimming away from any walls. Blind cave fish frequently touched walls when swimming alongside them, indicating that they use both tactile and hydrodynamic information in this situation. We conclude that although hydrodynamic imaging can provide effective collision avoidance, it is a short-range sense that may often be used synergistically with direct touch.

Temporal patterns in ambient noise of biological origin from a shallow water temperate reef.

A systematic study of the ambient noise in the shallow coastal waters of north-eastern New Zealand shows large temporal variability in acoustic power levels between seasons, moon phase and the time of day. Ambient noise levels were highest during the new moon and the lowest during the full moon. Ambient noise levels were also significantly higher during summer and lower during winter. Bandpass filtering (700-2,000 Hz and 2-15 kHz), combined with snap counts and data from other studies show that the majority of the sound intensity increases could be attributed to two organisms: the sea urchin and the snapping shrimp. The increased intensity of biologically produced sound during dusk, new moon and summer could enhance the biological signature of a reef and transmit it further offshore. Ambient noise generated from the coast, especially reefs, has been implicated as playing a role in guiding pelagic post-larval fish and crustaceans to settlement habitats. Determining a causal link between temporal increases in ambient noise and higher rates of settlement of reef fish and crustaceans would provide support for the importance of ambient underwater sound in guiding the settlement of these organisms.