Neural circuit mechanisms for steering control in walkingDrosophila

Abstract

During navigation, the brain must continuously integrate external guidance cues with internal spatial maps to update steering commands. However, it has been difficult to link spatial maps with motor control. Here we identify descending "steering" neurons in the Drosophila brain that lie two synapses downstream from the brain's heading direction map in the central complex. These steering neurons predict behavioral turns caused by microstimulation of the spatial map. Moreover, these neurons receive "direct" sensory input that bypasses the central complex, and they predict steering evoked by multimodal stimuli. Unilateral activation of these neurons can promote turning, while bilateral silencing interferes with body and leg movements. In short, these neurons combine internal maps with external cues to predict and influence steering. They represent a key link between cognitive maps, which use an abstract coordinate frame, and motor commands, which use a body-centric coordinate frame.

A connectome of theDrosophilacentral complex reveals network motifs suitable for flexible navigation and context-dependent action selection

“…To define output pathways, we began by examining the projection patterns of all core CX neuron types that have a significant number of presynaptic terminals in other brain regions ( Figure 54A, see Materials and Methods for details on significance test). These neurons target a narrow column around the CX that extends through the BU, GA, CRE, LAL, SPS, WED, RUB, ROB, SMP, SLP, IPS and SPS ( Figure 54A,B), as partially described in previous studies (Hanesch et al, 1989;Li et al, 2020;Lin et al, 2013;Rayshubskiy et al, 2020;Wolff et al, 2015;Wolff and Rubin, 2018). The neural projections and synapse locations within these regions appear to largely segregate by type (see Figure 54B).…”

“…This influence may be achieved not only by directly regulating motor pathways, but also by modulating the gain and tuning of early sensory pathways. To this end, the CX is well known to play an important role in the initiation and direction of movement (Bender et al, 2010;Guo and Ritzmann, 2013;Harley and Ritzmann, 2010;Kathman et al, 2014;Krause et al, 2019;Martin et al, 2015;Poeck et al, 2008;Rayshubskiy et al, 2020;Strauss, 2002;Strauss and Heisenberg, 1993;Triphan et al, 2010;Triphan et al, 2012). Different CX neurons make vastly different contributions to downstream networks ( Figure 59A), reflecting their unequal number of synapses ( Figure 54C), number of downstream targets ( Figure 55E) and contribution to CX-to-CX loops ( Figure 57A, Figure 57-figure supplement 1A).…”

Auditory Activity is Diverse and Widespread Throughout the Central Brain ofDrosophila

“…Adjusting our paradigm to drive such responses 49 , might uncover behavioral modulation of auditory activity. Alternatively, behavioral modulation of auditory responses may occur primarily in motor areas, such as the central complex or areas containing projections of descending neurons 50 . Further dissection of the sources of this variability would require capturing more brain activity simultaneously in behaving animals, while not significantly compromising spatial resolution.…”

Two Parallel Pathways Mediate Olfactory-Driven Backward Locomotion

“…For instance, optogenetic activation of TLAs while blocking MDNs 20 resulted in a residual backward walking component. In addition, backward movement was observed in association with a large membrane voltage difference between two non-MDN descending neurons 46 . Taken together, it seems that rather than a single command circuit originating in MDNs, there is at least one additional neural circuit the can mediate backward locomotion.…”

“…Having unequivocally identified MooSEZ as underlying GH146 II -GAL4 mediated backward locomotion we reconstructed its structure. MooSEZ morphology implies dendritic regions mostly in the SEZ, and putative presynaptic projections in the lower lateral accessory lobe (LAL) 46 located posterior to the AL and extending lateroventrally 47 -a major input region of MDNs 19 . The putative presynaptic arborizations are organized in a characteristic 2-dimensional vertical sheet that slopes from anterolateral to posteriomedial ( Figure 5B).…”