The insect central complex and the neural basis of navigational strategies

Abstract

Oriented behaviour is present in almost all animals, indicating that it is an ancient feature that has emerged from animal brains hundreds of millions of years ago. Although many complex navigation strategies have been described, each strategy can be broken down into a series of elementary navigational decisions. In each moment in time an animal has to compare its current heading with its desired direction and compensate for any mismatch by producing a steering response either to the right or to the left. Different from reflex driven movements, target directed navigation is not only initiated in response to sensory input, but also takes into account previous experience and motivational state. Once a series of elementary decisions are chained together to form one of many coherent navigation strategies, the animal can pursue a navigational target, e.g. a food source, a nest entrance, or a constant flight direction during migrations. Insects show a great variety of complex navigation behaviours and, owing to their small brains, the pursuit of the neural circuits controlling navigation has made substantial progress over the last years. A brain region as ancient as insects themselves, called the central complex, has emerged as the likely navigation centre of the brain. Research across many species has shown that the central complex contains the circuitry that might comprise the neural substrate of elementary navigational decisions. While this region is also involved in a wide range of other functions, we hypothesise in this review that its role in mediating the animal’s next move during target directed behaviour is its ancestral function, around which other functions have been layered over the course of evolution.

Prominent Inhibitory Projections Guide Sensorimotor Computation: An Invertebrate Perspective

“…Over time, the basic circuit elements evolve into more complex, parallel circuit loops that enable advanced multimodal computation, integration of mnemonic information, and executive control for top-down regulation of the www.advancedsciencenews.com www.bioessays-journal.com sensorimotor control (see Figure 2 for a phylogenetic view on the circuits from the sea slug to fruit fly). [18,108,109] The central complex (CX) is a point of convergence, having many inputs from sensorimotor circuits, with only a few outputs to guide flight pathways. Here, sensory information (light and vestibular) converges on the interneurons, but there is also reciprocal inhibition between the hair cells and photoreceptors.…”

“…The sea slug, H. crassicornis, has a simple nervous system. [18,108,109] www.advancedsciencenews.com www.bioessays-journal.com seeded sensorimotor loops. I, II, III, interneurons; VCMN, ventral contraction motor neuron; VP, ventral pedal.…”

“…[100] Figure 2 shows a concise representation of the fly sensorimotor loops. [18,108,109] The central complex (CX) is a point of convergence, having many inputs from sensorimotor circuits, with only a few outputs to guide flight pathways. [100,101] The CX is composed of a number of structures, including the protocerebral bridge (PB), the fan-shaped body (FB), and the ellipsoid body as well as various substructures (Figure 2).…”

“…[1,2] It has been speculated that the first neurons evolved to provide fast electrical signal propagation to control navigation, [3] which ultimately gave rise to organisms that employ muscle-based locomotion as cilia evolved into a sensory organ. [15][16][17][18][19][20] Here, we focus on the networks that have evolved to provide such sensorimotor control to address general principles of sensorimotor computation from a neural circuit perspective, with the focus being on Caenorhabditis elegans (C. elegans). [7][8][9] Although sensorimotor computation commonly leads to navigation (as well as other forms of motor control including vocalization and vocal communication [10][11][12][13][14] ), we refrain from discussing the circuits of navigation, which are reviewed elsewhere.…”

“…[7][8][9] Although sensorimotor computation commonly leads to navigation (as well as other forms of motor control including vocalization and vocal communication [10][11][12][13][14] ), we refrain from discussing the circuits of navigation, which are reviewed elsewhere. [15][16][17][18][19][20] Here, we focus on the networks that have evolved to provide such sensorimotor control to address general principles of sensorimotor computation from a neural circuit perspective, with the focus being on Caenorhabditis elegans (C. elegans). By focusing our arguments on three key highlights, we show that C. elegans, like all animals, require sensorimotor integration to generate action and explore the computational roles of inhibitory neurons that allow adaptive sensorimotor computations.…”