Ascending neurons convey behavioral state to integrative sensory and action selection brain regions

Abstract

Knowing one’s own behavioral state has long been theorized as critical for contextualizing dynamic sensory cues and identifying appropriate future behaviors. Ascending neurons (ANs) in the motor system that project to the brain are well positioned to provide such behavioral state signals. However, what ANs encode and where they convey these signals remains largely unknown. Here, through large-scale functional imaging in behaving animals and morphological quantification, we report the behavioral encoding and brain targeting of hundreds of genetically identifiable ANs in the adult fly, Drosophila melanogaster. We reveal that ANs encode behavioral states, specifically conveying self-motion to the anterior ventrolateral protocerebrum, an integrative sensory hub, as well as discrete actions to the gnathal ganglia, a locus for action selection. Additionally, AN projection patterns within the motor system are predictive of their encoding. Thus, ascending populations are well poised to inform distinct brain hubs of self-motion and ongoing behaviors and may provide an important substrate for computations that are required for adaptive behavior.

Global change in brain state during spontaneous and forced walk in Drosophila is composed of combined activity patterns of different neuron classes

“…For instance, DNs receive input from regions of the brain that are innervated by outputs from higher brain regions such as the MB and CC ( Hsu and Bhandawat, 2016 ). DN and AN innervation of the GNG is consistent with an important role of the GNG in motor control and motor feedback integration ( Chen et al, 2023 ; Tsubouchi et al, 2017 ). How anatomical connectivity relates to activity in widespread neural networks is not clear.…”

“…First, the activity could arise initially in superior decision-making areas and then spreads across the brain (top-down) or, second, activity is initiated by motor activity and proprioception (bottom-up) and then distributes to higher brain areas. In the latter case, activity would originate in the VNC and move to basal regions of the brain, i.e., the GNG, via ascending neurons (ANs) ( Chen et al, 2023 ; Tsubouchi et al, 2017 ). While our component analysis of data recorded at 30 Hz identified several putative ‘top-down’ components active before walk onset, most activity was more consistent with a ‘bottom-up’ scenario ( Figures 1 and 6 and Figure 6—figure supplements 1 and 2 ).…”

“…The AVLP receives input from ANs from the VNC conveying somatosensory information from the legs ( Tsubouchi et al, 2017 ). Furthermore, calcium imaging revealed a spatial map for the AVLP and WED with neurons responding primarily to movement of fore-, mid-, or hindlegs ( Chen et al, 2023 ; Tsubouchi et al, 2017 ) , and the AVLP contains several descending neurons projecting toward the VNC ( Namiki et al, 2022 ; Namiki et al, 2018 ). Serotonin inhibition in the AVLP could thus also be affecting a sensorimotor loop.…”

“…Less was known regarding the type, connectivity and function of the likely dozens or more AN in Drosophila , but screening approaches and advanced imaging techniques have shed light on some of them ( Allen et al, 2020 ; Sen et al, 2019 ). In particular, a very recent study analyzed behavior-related activity of dozens of ANs labeled with specific Gal4 lines ( Chen et al, 2023 ) and came to the complementary conclusion that ANs innervating regions such as the AVLP and GNG are poised to convey behavioral state and self-motion to several brain regions.…”

NeuroMechFly v2, simulating embodied sensorimotor control in adult Drosophila

“…Notably, important behaviors, including those involving the control of wings/halteres (e.g., flight), abdomen (e.g., egg-laying), and proboscis (e.g., feeding) are not yet demonstrated but are supported within this framework. Additionally, signals like ascending motor-related feedback 79 and those encoding internal states 33 or learning-based 72 changes in sensory valence can be easily incorporated into user-defined controllers.…”