The function of the hands is inextricably linked to cutaneous mechanosensation, both in touch and in how hand movement and posture (proprioception) are controlled. The structure and behavior of hands ...and distal forelimbs of other vertebrates have been evolutionarily shaped by these mechanosensory functions. The distal forelimb of tetrapod vertebrates is homologous to the pectoral fin rays and membrane of fishes. Fish fins demonstrate similar mechanosensory abilities to hands and other distal tetrapod forelimbs in touch and proprioception. These results indicate that vertebrates were using the core mechanosensory inputs, such as fast adapting and slow adapting nerve responses, to inform fin and limb function and behavior before their diversification in fish and tetrapod lineages.
•Cutaneous mechanosensation is important for distal limb function across vertebrates.•Basic mechanosensory physiology is common to bony fish fins and tetrapod hands.•Bony vertebrates have a shared evolutionary origin of cutaneous mechanosensation.•Evolution of fin and hand behaviors has been shaped from this mechanosensory origin.
Octopuses are remarkable in their ability to use many arms together during behavior (e.g., see Levy et al., 1 Mather,2 Byrne et al.,3 and Hanlon et al.4). Arm responses and multi-arm coordination can ...occur without engagement of major brain regions,5 which indicates the importance of local proprioceptive responses and peripheral connections. Here, we examine the intramuscular nerve cords (INCs),6,7,8,9 the key proprioceptive anatomy in the arms. INCs are understood to include proprioceptive neurons, multipolar neurons, and motoneurons (reviewed by Graziadei10) and are thought to contribute to structuring whole-arm movement.11 There are four INCs running the full length of each arm (e.g., see Guérin-Ganivet,6 Martoja and May,8 and Graziadei9); we focused on the pair closest to the suckers, called the oral INCs. In tracking the oral INCs, we found that they extend proximally and continue beyond the arm, through the arm’s base. Each oral INC bypasses two adjacent arms and is continuous with the nearer oral INC of the third arm over. As a result, an arm connects through oral INC pathways to arms that are two arms away to the right and left of it. In addition to connecting distant arms, nerve fibers project from the central region of the INCs, suggesting function in local tissues. The other two INCs, paired aboral INCs, also extend proximally beyond the arm’s base with trajectories suggestive of the oral INC pattern. These data identify previously unknown regions of the INCs that link distant arms, creating anatomical connections. They suggest potential INC proprioceptive function in extra-arm tissues and contribute to an understanding of embodied organization for octopus behavioral control.12,13,14,15
•Octopus bimaculoides’ intramuscular nerve cords extend proximally from the arm•Oral intramuscular nerve cords are anatomically continuous between distant arms•A nerve cord bypasses two arms connecting to the third arm over•The same anatomical connection pattern occurs for all eight arms
Kuuspalu et al. describe direct neural connections between distant arms in octopuses. Each of the paired oral intramuscular nerve cords in an arm is continuous with a cord that is three arms over. This pattern occurs for all arms and demonstrates potential paths for inter-arm communication outside of central integrating structures like the brain.
The reticulospinal Mauthner cells (M-cells) of the startle circuit have been considered to be dedicated to one basic motor output and the C-type startle response in fish. The neural circuit ...underlying the C-start, a startle behavior in which the fish forms a “C”-shaped body bend has been described in depth in goldfish and zebrafish 1, 2 and is thought to occur in other species 3, 4. However, previous research has shown that some species can perform a second type of startle called the S-start 5–7. This startle response, in which the first movement creates an “S”-shaped body bend achieved with regional muscle activity on left and right sides, cannot be explained by M-cell circuit models. Here we use larval zebrafish to examine the S-start circuit. Since S-starts are elicited through tail stimulation 5–7 and ablating M-cells abolishes short-latency tail-elicited startles 8, 9, we hypothesized that M-cell activity was necessary for S-start generation. Our findings show that the M-cells fire simultaneously to generate the S-start. However, simultaneous M-cell spikes generated through direct current injection were not sufficient to generate S-starts. Through recordings of motoneurons, inhibitory interneurons, and sensory neurons, we uncover a mechanism for generating alternative startle behaviors; local sensory inputs drive inhibitory interneuron activity, which inhibits caudal motoneurons and pre-conditions their excitability prior to the arrival of M-cell spikes in the tail. We suggest that this motoneuron hyperpolarization can bias motor output to left or right sides, determining whether the fish performs a C-start or an S-start behavior.
•Bilateral M-cells activity can drive C-starts and S-starts in tail-elicited startles•Caudal sensory neurons excite local caudal inhibitory interneurons•Inhibitory interneurons rapidly hyperpolarize local motoneurons•Motoneuron inhibition shapes motor output resulting from M-cell spikes
Larval zebrafish respond to tail stimulation with alternative startle behaviors, C-starts or S-starts. Liu and Hale show that bilateral M-cell activity and caudal spinal cord circuits drive S-starts. They find that sensory inputs to caudal spinal cord inhibit motoneurons before M-cells can excite them, shaping motor output and body bending.
The brain has been shaped by evolution, and its connectome reflects that history. Comparative neuroscience research, framed by evolutionary relationships, is key to interpreting connectome ...organization and can address fundamental circuit questions that are not accessible through single-species connectomics efforts.
In this NeuroView, Hale discusses how comparative neuroscience research is key to interpreting connectome organization and can address fundamental circuit questions that are not accessible through single-species connectomics efforts.
Hale expresses commentary on the study by Mohren et al, inspired by the biological instrumentation of mechanosensory surfaces, developed and implemented computational approaches that provide insight ...on the biology and engineering of sparse sensing from wings. The researchers looked to the wings of insects, where fast and controlled flight movements are informed, in part, by mechanosensory cells called campaniform sensilla located on the wings to understand and innovate strategies for design of mechanosensory systems with sparse sensing.
The biomechanics of animal limbs has evolved to meet the functional demands for movement associated with different behaviors and environments. Effective movement relies not only on limb mechanics but ...also on appropriate mechanosensory feedback. By comparing sensory ability and mechanics within a phylogenetic framework, we show that peripheral mechanosensation has evolved with limb biomechanics, evolutionarily tuning the neuromechanical system to its functional demands. We examined sensory physiology and mechanics of the pectoral fins, forelimb homologs, in the fish family Labridae. Labrid fishes exhibit extraordinary morphological and behavioral diversity and use pectoral fin-based propulsion with fins ranging in shape from high aspect ratio (AR) wing-like fins to low AR paddle-like fins. Phylogenetic character analysis demonstrates that high AR fins evolved independently multiple times in this group. Four pairs of species were examined; each included a plesiomorphic low AR and a high AR species. Within each species pair, the high AR species demonstrated significantly stiffer fin rays in comparison with the low AR species. Afferent sensory nerve activity was recorded during fin ray bending. In all cases, afferents of stiffer fins were more sensitive at lower displacement amplitudes, demonstrating mechanosensory tuning to fin mechanics and a consistent pattern of correlated evolution. We suggest that these data provide a clear example of parallel evolution in a complex neuromechanical system, with a strong link between multiple phenotypic characters: pectoral fin shape, swimming behavior, fin ray stiffness, and mechanosensory sensitivity.
Fins of fishes provide many examples of structures that are beautifully designed to power and control movement in water; however, some species also use their fins for substrate-associated behaviors ...where interactions with solid surfaces are key. Here we examine how the pectoral fins of ray-finned fish with these multifunctional behavioral demands, in water and on solid surfaces, are structured and function. We subdivide fins used in swimming and substrate contact into two general morphological categories, regionalized vs. generalized fins. Regionalized fins have ventral rays that are free from connecting membrane or in which that membrane is reduced. Dorsally they maintain a more typical membranous fin. While all pectoral fins vary somewhat in their morphology from leading to trailing edge, generalized fins do not have the substantial membrane loss between rays that is seen in regionalized fins and the distal edge anatomy changes gradually along its margin. We add a new case study in regionalized fins with the dwarf hawkfish (Cirrhitichthys falco). Hawkfishes are most often found perching and moving on structures in their environments. During perching, the free ventral rays are in contact with the substrate and splayed. We found that unlike other fish with regionalized pectoral fins, hawkfish maintain use of the dorsal membranous region of its pectoral fin for rhythmic swimming. We found that typically hawkfish bend their ventral free rays under, toward the medial hemitrichs or hold them straight during substrate-associated postures. This appears also to be the case for the ventral free rays of other species with regionalized fins. Generalized fin use for substrate contact was reviewed in round gobies (Neogobius melanostomus). In addition, although their lobe fins are not representative of ray-finned fish anatomy, we explored fin contact on submerged substrates in the Senegal bichir (Polypterus senegalus), which has a generalized distal fin (no free fin rays or distinct membrane regions). Both groups use their pectoral fins for swimming. During substrate-based postures, unlike hawkfish, their distal rays generally bend outward toward the lateral hemitrichs and a large swath of the fin membrane can contact the surface. The alternative demands on multifunctional fins suggest specialization of the mechanosensory system. We review mechanosensation related to fin movement and surface contact. These alternative regionalized and generalized strategies for serving aquatic and substrate-based functions underwater provide opportunities to further investigate specializations, including sensory structures and systems, that accompany the evolution of substrate-based behaviors in vertebrates.
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