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.
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The self as part of the sensory ecology: how behavior affects sensation from the inside out
Insects exhibit remarkable sensory , motor capabilities to successfully navigate their environment. As insects move, they activate sensory afferents. Hence, insects are inextricably part of their sensory ecology. Insects must correctly attribute self -versus external sources of sensory activation to make adaptive behavioral choices. This is achieved via corollary discharge circuits (CDCs), motor-to-sensory neuronal pathways providing predictive motor signals to sensory networks to coordinate sensory processing within the context of ongoing behavior. While CDCs provide predictive motor signals, their underlying mechanisms of action and functional consequences are diverse. Here, we describe inferred CDCs and identified corollary discharge interneurons (CDIs) in insects, highlighting their anatomical commonalities and our limited understanding of their synaptic integration into the nervous system. By using connectomics information, we demonstrate that the complexity with which identified CDIs integrate into the central nervous system (CNS) can be revealed.
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- Award ID(s):
- 2127379
- PAR ID:
- 10503336
- Editor(s):
- Hempel de Ibarra, N; Mustard, J.
- Publisher / Repository:
- Current Opinion in Insect Science
- Date Published:
- Journal Name:
- Current Opinion in Insect Science
- Volume:
- 58
- Issue:
- C
- ISSN:
- 2214-5745
- Page Range / eLocation ID:
- 101053
- Subject(s) / Keyword(s):
- induced air-flow sphinx moth corollary discharge projection neurons flight behavior antennal lobes flying insects cricket gaba interneurons
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)Sensory feedback during movement entails sensing a mix of externally- and self-generated stimuli (respectively, exafference and reafference). In many peripheral sensory systems, a parallel copy of the motor command, a corollary discharge, is thought to eliminate sensory feedback during behaviors. However, reafference has important roles in motor control, because it provides real-time feedback on the animal’s motions through the environment. In this case, the corollary discharge must be calibrated to enable feedback while avoiding negative consequences like sensor fatigue. The undulatory motions of fishes’ bodies generate induced flows that are sensed by the lateral line sensory organ, and prior work has shown these reafferent signals contribute to the regulation of swimming kinematics. Corollary discharge to the lateral line reduces the gain for reafference, but cannot eliminate it altogether. We develop a data-driven model integrating swimming biomechanics, hair cell physiology, and corollary discharge to understand how sensory modulation is calibrated during locomotion in larval zebrafish. In the absence of corollary discharge, lateral line afferent units exhibit the highly heterogeneous habituation rates characteristic of hair cell systems, typified by decaying sensitivity and phase distortions with respect to an input stimulus. Activation of the corollary discharge prevents habituation, reduces response heterogeneity, and regulates response phases in a narrow interval around the time of the peak stimulus. This suggests a synergistic interaction between the corollary discharge and the polarization of lateral line sensors, which sharpens sensitivity along their preferred axes. Our integrative model reveals a vital role of corollary discharge for ensuring precise feedback, including proprioception, during undulatory locomotion.more » « less
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Baden, Tom (Ed.)Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral nervous system cancels reafference to protect sensors and the central nervous system from being fatigued and overwhelmed by self-generated feedback. However, cancellation also limits the feedback that contributes to an animal’s awareness of its body position and motion within the environment, the sense of proprioception. We propose that, rather than cancellation, CD to the fish lateral line organ restructures reafference to maximize proprioceptive information content. Fishes’ undulatory body motions induce reafferent feedback that can encode the body’s instantaneous configuration with respect to fluid flows. We combined experimental and computational analyses of swimming biomechanics and hair cell physiology to develop a neuromechanical model of how fish can track peak body curvature, a key signature of axial undulatory locomotion. Without CD, this computation would be challenged by sensory adaptation, typified by decaying sensitivity and phase distortions with respect to an input stimulus. We find that CD interacts synergistically with sensor polarization to sharpen sensitivity along sensors’ preferred axes. The sharpening of sensitivity regulates spiking to a narrow interval coinciding with peak reafferent stimulation, which prevents adaptation and homogenizes the otherwise variable sensor output. Our integrative model reveals a vital role of CD for ensuring precise proprioceptive feedback during undulatory locomotion, which we term external proprioception.more » « less
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Appropriate generalization of learned responses to new situations is vital for adaptive behavior. We provide a circuit-level account of generalization in the electrosensory lobe (ELL) of weakly electric mormyrid fish. Much is already known in this system about a form of learning in which motor corollary discharge signals cancel responses to the uninformative input evoked by the fish’s own electric pulses. However, for this cancellation to be useful under natural circumstances, it must generalize accurately across behavioral regimes, specifically different electric pulse rates. We show that such generalization indeed occurs in ELL neurons, and develop a circuit-level model explaining how this may be achieved. The mechanism involves regularized synaptic plasticity and an approximate matching of the temporal dynamics of motor corollary discharge and electrosensory inputs. Recordings of motor corollary discharge signals in mossy fibers and granule cells provide direct evidence for such matching.more » « less
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Animals utilize a number of neuronal systems to produce locomotion. One type of sensory organ that contributes in insects is the campaniform sensillum (CS) that measures the load on their legs. Groups of the receptors are found on high stress regions of the leg exoskeleton and they have significant effects in adapting walking behavior. Recording from these sensors in freely moving animals is limited by technical constraints. To better understand the load feedback signaled by CS to the nervous system, we have constructed a dynamically scaled robotic model of the Carausius morosus stick insect middle leg. The leg steps on a treadmill and supports weight during stance to simulate body weight. Strain gauges were mounted in the same positions and orientations as four key CS groups (Groups 3, 4, 6B, and 6A). Continuous data from the strain gauges were processed through a previously published dynamic computational model of CS discharge. Our experiments suggest that under different stepping conditions (e.g., changing “body” weight, phasic load stimuli, slipping foot), the CS sensory discharge robustly signals increases in force, such as at the beginning of stance, and decreases in force, such as at the end of stance or when the foot slips. Such signals would be crucial for an insect or robot to maintain intra- and inter-leg coordination while walking over extreme terrain.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1016/j.cois.2023.101053
