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Flexible control of pectoral appendages enables motor behaviors of vastly different strength, speed, and amplitude, as in a human playing the piano or throwing a ball. Such control necessitates a fine-tuned, coordinated activation of motoneurons, which is facilitated by spatially ordered motoneuron pools in mammals. While differently sized neurons are known to contribute to different strengths of pectoral movements, it remains unclear how these pectoral motor pools are organized in less complex pectoral systems as those of teleost fish. We show how pectoral motor control can be extended to increase the speed- and amplitude-range of motor behaviors by investigating anatomical and physiological features of pectoral motoneurons and the motor pools they form in freshwater hatchet fish, well-known for their pectoral aerial escape response. Through the differentiation of one motor pool, the pectoral motor network of hatchet fish acquired additional flexibility to enable specific control of vastly different amplitudes, velocities, and strengths. Similar neuronal organization patterns have been described for controlling fast, intermediate, and slow axial muscles in zebrafish and in tetrapod motor systems controlling pectoral limbs. We show that hatchet fish share organizational principles of their pectoral motor pools with those found in other motor networks in both teleosts and tetrapods. Our data thus suggest that principles of spatial and physiological differentiation of motor pools associated with different pectoral muscles and behaviors might be deeply homologous between actinopterygian and sarcopterygian vertebrates., Competing Interests: Competing interests statement:The authors declare no competing interest.

The evolution of novel motor behaviors requires modifications in the central pattern generators (CPGs) controlling muscle activity. How such changes gradually lead to novel behaviors remains enigmatic due to the long time course of evolution. Rattlesnakes provide a unique opportunity to investigate how a locomotor CPG was evolutionarily modified to generate a novel behavior-in this case, acoustic signaling. We show that motoneurons (MNs) in the body and tail spinal cord of rattlesnakes possess fundamentally different physiological characteristics, which allow MNs in the tail to integrate and transmit CPG output for controlling superfast muscles with high temporal precision. Using patch-clamp electrophysiology, we demonstrate that these differences in locomotor and rattle MNs are mainly determined by KV7 2/3 potassium channels. However, although KV7 2/3 exerted a significantly different influence on locomotor and rattle MN physiology, single-cell RNA-seq unexpectedly did not reveal any differences in KV7 2/3 channels' expression. VIDEO ABSTRACT., Competing Interests: Declaration of interests The authors declare no conflict of interests., (Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.)

Pit vipers detect infrared (IR) radiation with loreal pit organs [1] that are connected to the hindbrain by trigeminal nerve fibers [2-4]. The pattern of central afferent termination forms a topographical representation of the sensory periphery within the nucleus of the lateral descending trigeminal tract (LTTD) [4-7]. All LTTD neurons project to another specialized, ipsilateral hindbrain area, the nucleus reticularis caloris (RC) [8-11], before IR signals are integrated with visual signals in the optic tectum [12, 13]. Pit-organ-innervating afferent fibers provoke in individual LTTD neurons a direct, robust spike activity upon peripheral activation [7, 14]. This discharge is truncated by an indirect, delayed synaptic inhibition from afferent fibers of adjacent sensory areas through parallel microcircuitry that converges with afferent fibers onto the same target neurons [7]. Here, we determined the impact of this interaction on IR contrast enhancement and/or motion detection in LTTD and RC neurons using isolated whole-brain preparations of rattlesnakes with intact pit organs. Simulated and real IR source motion provoked weak directional tuning of the discharge in LTTD neurons and RC neurons expressed a strong, motion-direction-differentiating activity. The hierarchically increasing motion sensitivity potentially derives from a direction-specific inhibition or spike frequency adaptation of LTTD neuronal discharge that becomes further pronounced by convergent projections onto individual RC neurons. The emerging signaling pattern complies with contrast enhancement (LTTD) and extraction of movement-related signals (RC), thereby forming a motion detection mechanism that encodes moving IR sources relative to the ambient temperature [14]., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

Pitvipers have a specialized sensory system in the upper jaw to detect infrared (IR) radiation. The bilateral pit organs resemble simple pinhole cameras that map IR objects onto the sensory epithelium as blurred representations of the environment. Trigeminal afferents transmit information about changing temperature patterns as neuronal spike discharge in a topographic manner to the hindbrain nucleus of the lateral descending trigeminal tract (LTTD). A presumed, yet so far unknown neuronal connectivity within this central nucleus exerts a synaptic computation that constrains the relatively large receptive field of primary afferent fibers. Here, we used intracellular recordings of LTTD neurons in isolated rattlesnake brains to decipher the spatio-temporal pattern of excitatory and inhibitory responses following electrical stimulation of single and multiple peripheral pit organ-innervating nerve branches. The responses of individual neurons consisted of complex spike sequences that derived from spatially and temporally specific interactions between excitatory and inhibitory synaptic inputs from the same as well as from adjacent peripheral nerve terminal areas. This pattern complies with a central excitation that is flanked by a delayed lateral inhibition, thereby enhancing the contrast of IR sensory input, functionally reminiscent of the computations for contrast enhancement in the peripheral visual system., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

Pit vipers (Crotalinae) have a specific sensory system that detects infrared radiation with bilateral pit organs in the upper jaw. Each pit organ consists of a thin membrane, innervated by three trigeminal nerve branches that project to a specific nucleus in the dorsal hindbrain. The known topographic organization of infrared signals in the optic tectum prompted us to test the implementation of spatiotopically aligned sensory maps through hierarchical neuronal levels from the peripheral epithelium to the first central site in the hindbrain, the nucleus of the lateral descending trigeminal tract (LTTD). The spatial organization of the anatomical connections was revealed in a novel in vitro whole-brain preparation of the western diamondback rattlesnake (Crotalus atrox) that allowed specific application of multiple neuronal tracers to identified pit-organ-supplying trigeminal nerve branches. After adequate survival times, the entire peripheral and central projections of fibers within the pit membrane and the LTTD became visible. This approach revealed a morphological partition of the pit membrane into three well-defined sensory areas with largely separated innervations by the three main branches. The peripheral segregation of infrared afferents in the sensory epithelium was matched by a differential termination of the afferents within different areas of the LTTD, with little overlap. This result demonstrates a topographic organizational principle of the snake infrared system that is implemented by maintaining spatially aligned representations of environmental infrared cues on the sensory epithelium through specific neuronal projections at the level of the first central processing stage, comparable to the visual system., (© 2014 Wiley Periodicals, Inc.)