An official website of the United States government
Natural behaviors are a coordinated symphony of motor acts that drive reafferent (self-induced) sensory activation. Individual sensors cannot disambiguate exafferent (externally induced) from reafferent sources. Nevertheless, animals readily differentiate between these sources of sensory signals to carry out adaptive behaviors through corollary discharge circuits (CDCs), which provide predictive motor signals from motor pathways to sensory processing and other motor pathways. Yet, how CDCs comprehensively integrate into the nervous system remains unexplored. Here, we use connectomics, neuroanatomical, physiological, and behavioral approaches to resolve the network architecture of two pairs of ascending histaminergic neurons (AHNs) in Drosophila, which function as a predictive CDC in other insects. Both AHN pairs receive input primarily from a partially overlapping population of descending neurons, especially from DNg02, which controls wing motor output. Using Ca2+ imaging and behavioral recordings, we show that AHN activation is correlated to flight behavior and precedes wing motion. Optogenetic activation of DNg02 is sufficient to activate AHNs, indicating that AHNs are activated by descending commands in advance of behavior and not as a consequence of sensory input. Downstream, each AHN pair targets predominantly non-overlapping networks, including those that process visual, auditory, and mechanosensory information, as well as networks controlling wing, haltere, and leg sensorimotor control. These results support the conclusion that the AHNs provide a predictive motor signal about wing motor state to mostly non-overlapping sensory and motor networks. Future work will determine how AHN signaling is driven by other descending neurons and interpreted by AHN downstream targets to maintain adaptive sensorimotor performance.
more »
« less
This content will become publicly available on July 1, 2026
Motor control on the move: from insights in insects to general mechanisms
This review discusses how the nervous system controls the complex body movements keeping animals up and running. In particular, we revisit how research in insects has shed light on motor control principles that govern movements across the animal kingdom. Starting with the organization and evolution of the insect nervous system, we discuss insights into the neuronal control of behaviors varying in complexity, including escape, flight, crawling, walking, grooming, and courtship. These behaviors share specific control features. For instance, central pattern-generating circuits (CPG), which reside in proximity to the motor neurons and muscles, support the generation of rhythmic motor activity. The number of CPGs involved depends on the complexity of the motor apparatus controlled, such as wing pairs for flight or six pairs of multisegmented legs for walking. The different control architectures are introduced with respect to their organization, topology, and operation. Sensory feedback plays a pivotal role in shaping CPG activity into a functional, well-coordinated motor output. The activity of motor circuits is orchestrated by descending neurons connecting the brain to the ventral nerve cord or spinal cord, which initiate, maintain, modulate, and terminate different actions. We therefore discuss the current understanding of descending control and the contributions of individual, command-like descending neurons and population codes. To highlight how insights in insects help discover fundamental motor control principles, we cross-reference findings from other animals, particularly vertebrates. In addition, we discuss methodological advances that enabled breakthroughs in motor control research, including neurogenetics and connectomics, and discuss key open questions.
more »
« less
- Award ID(s):
- 2015317
- PAR ID:
- 10627452
- Publisher / Repository:
- American Physiological Society
- Date Published:
- Journal Name:
- Physiological Reviews
- Volume:
- 105
- Issue:
- 3
- ISSN:
- 0031-9333
- Page Range / eLocation ID:
- 975 to 1031
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Summary Animals need to fine-control the speed and direction of locomotion to navigate complex and dynamic environments. To achieve this, they integrate multimodal sensory inputs with their internal drive to constantly adjust their motor output. This integration involves the interplay of neuronal populations across different hierarchical levels along the sensorimotor axis – from sensory, central, and modulatory neurons in the brain to descending neurons and motor networks in the nerve cord. Here, we characterize two populations of neurons that control distinct aspects of walking on different hierarchical levels inDrosophila. First, we usein-vivoelectrophysiological recordings to demonstrate that moonwalker descending neurons (MDN) integrate antennal touch to drive changes in walking direction from forward to backward. Second, we establish DopaMeander as an important component in the control of forward walking through a combination of optogenetic activation, silencing, connectomics, andin-vivorecordings. These dopaminergic modulatory neurons drive forward walking with increased turning, and the activity of individual neurons is correlated with ipsiversive turning. Hence, MDN and DopaMeander control opposite regimes of walking on different hierarchical levels. Computational models reveal that their activity predicts key parameters of spontaneous walking. Moreover, we find that both MDN and DopaMeander are gated out during flight. This suggests that neuronal populations across levels of control are modulated by the behavioral state to minimize cross-talk between motor programs.more » « less
-
Abstract In most complex nervous systems there is a clear anatomical separation between the nerve cord, which contains most of the final motor outputs necessary for behaviour, and the brain. In insects, the neck connective is both a physical and information bottleneck connecting the brain and the ventral nerve cord (VNC, spinal cord analogue) and comprises diverse populations of descending (DN), ascending (AN) and sensory ascending neurons, which are crucial for sensorimotor signalling and control. Integrating three separate EM datasets, we now provide a complete connectomic description of the ascending and descending neurons of the female nervous system ofDrosophilaand compare them with neurons of the male nerve cord. Proofread neuronal reconstructions have been matched across hemispheres, datasets and sexes. Crucially, we have also matched 51% of DN cell types to light level data defining specific driver lines as well as classifying all ascending populations. We use these results to reveal the general architecture, tracts, neuropil innervation and connectivity of neck connective neurons. We observe connected chains of descending and ascending neurons spanning the neck, which may subserve motor sequences. We provide a complete description of sexually dimorphic DN and AN populations, with detailed analysis of circuits implicated in sex-related behaviours, including female ovipositor extrusion (DNp13), male courtship (DNa12/aSP22) and song production (AN hemilineage 08B). Our work represents the first EM-level circuit analyses spanning the entire central nervous system of an adult animal.more » « less
-
Abstract This article is a historical perspective on how the study of the neuromechanics of insects and other arthropods has inspired the construction, and especially the control, of hexapod robots. Many hexapod robots’ control systems share common features, including: 1. Direction of motor output of each joint (i.e. to flex or extend) in the leg is gated by an oscillatory or bistable gating mechanism; 2. The relative phasing between each joint is influenced by proprioceptive feedback from the periphery (e.g. joint angles, leg load) or central connections between joint controllers; and 3. Behavior can be directed (e.g. transition from walking along a straight path to walking along a curve) via low-dimensional, broadly-acting descending inputs to the network. These distributed control schemes are inspired by, and in some robots, closely mimic the organization of the nervous systems of insects, the natural hexapods, as well as crustaceans. Nearly a century of research has revealed organizational principles such as central pattern generators, the role of proprioceptive feedback in control, and command neurons. These concepts have inspired the control systems of hexapod robots in the past, in which these structures were applied to robot controllers with neuromorphic (i.e. distributed) organization, but not neuromorphic computational units (i.e. neurons) or computational hardware (i.e. hardware-accelerated neurons). Presently, several hexapod robots are controlled with neuromorphic computational units with or without neuromorphic organization, almost always without neuromorphic hardware. In the near future, we expect to see hexapod robots whose controllers include neuromorphic organization, computational units, and hardware. Such robots may exhibit the full mobility of their insect counterparts thanks to a ‘biology-first’ approach to controller design. This perspective article is not a comprehensive review of the neuroscientific literature but is meant to give those with engineering backgrounds a gentle introduction into the neuroscientific principles that underlie models and inspire neuromorphic robot controllers. A historical summary of hexapod robots whose control systems and behaviors use neuromorphic elements is provided. Robots whose controllers closely model animals and may be used to generate concrete hypotheses for future animal experiments are of particular interest to the authors. The authors hope that by highlighting the decades of experimental research that has led to today’s accepted organization principles of arthropod nervous systems, engineers may better understand these systems and more fully apply biological details in their robots. To assist the interested reader, deeper reviews of particular topics from biology are suggested throughout.more » « less
-
Mammalian locomotion is generated by central pattern generators (CPGs) in the spinal cord, which produce alternating flexor and extensor activities controlling the locomotor movements of each limb. Afferent feedback signals from the limbs are integrated by the CPGs to provide adaptive control of locomotion. Responses of CPG-generated neural activity to afferent feedback stimulation have been previously studied during fictive locomotion in immobilized cats. Yet, locomotion in awake, behaving animals involves dynamic interactions between central neuronal circuits, afferent feedback, musculoskeletal system, and environment. To study these complex interactions, we developed a model simulating interactions between a half-center CPG and the musculoskeletal system of a cat hindlimb. Then, we analyzed the role of afferent feedback in the locomotor adaptation from a dynamic viewpoint using the methods of dynamical systems theory and nullcline analysis. Our model reproduced limb movements during regular cat walking as well as adaptive changes of these movements when the foot steps into a hole. The model generates important insights into the mechanism for adaptive locomotion resulting from dynamic interactions between the CPG-based neural circuits, the musculoskeletal system, and the environment.more » « less
