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Biological Mechanisms for Learning: A Computational Model of Olfactory Learning in the Manduca sexta Moth, With Applications to Neural Nets.

ABSTRACT: The insect olfactory system, which includes the antennal lobe (AL), mushroom body (MB), and ancillary structures, is a relatively simple neural system capable of learning. Its structural features, which are widespread in biological neural systems, process olfactory stimuli through a cascade of networks where large dimension shifts occur from stage to stage and where sparsity and randomness play a critical role in coding. Learning is partly enabled by a neuromodulatory reward mechanism of octopamine stimulation of the AL, whose increased activity induces synaptic weight updates in the MB through Hebbian plasticity. Enforced sparsity in the MB focuses Hebbian growth on neurons that are the most important for the representation of the learned odor. Based upon current biophysical knowledge, we have constructed an end-to-end computational firing-rate model of the Manduca sexta moth olfactory system which includes the interaction of the AL and MB under octopamine stimulation. Our model is able to robustly learn new odors, and neural firing rates in our simulations match the statistical features of in vivo firing rate data. From a biological perspective, the model provides a valuable tool for examining the role of neuromodulators, like octopamine, in learning, and gives insight into critical interactions between sparsity, Hebbian growth, and stimulation during learning. Our simulations also inform predictions about structural details of the olfactory system that are not currently well-characterized. From a machine learning perspective, the model yields bio-inspired mechanisms that are potentially useful in constructing neural nets for rapid learning from very few samples. These mechanisms include high-noise layers, sparse layers as noise filters, and a biologically-plausible optimization method to train the network based on octopamine stimulation, sparse layers, and Hebbian growth.

SUBMITTER: Delahunt CB

PROVIDER: S-EPMC6306094 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundInsects detect a multitude of odors using a broad array of phenotypically distinct olfactory organs referred to as olfactory sensilla. Each sensillum contains one to several sensory neurons and at least three support cells; these cells arise from mitotic activities from one or a small group of defined precursor cells. Sensilla phenotypes are defined by distinct morphologies, and specificities to specific odors; these are the consequence of developmental programs expressed by associated neurons and support cells, and by selection and expression of subpopulations of olfactory genes encoding such proteins as odor receptors, odorant binding proteins, and odor degrading enzymes.Methodology/principal findingsWe are investigating development of the olfactory epithelium of adult M. sexta, identifying events which might establish sensilla phenotypes. In the present study, antennal tissue was examined during the first three days of an 18 day development, a period when sensory mitotic activity was previously reported to occur. Each antenna develops as a cylinder with an outward facing sensory epithelium divided into approximately 80 repeat units or annuli. Mitotic proliferation of sensory cells initiated about 20-24 hrs after pupation (a.p.), in pre-existing zones of high density cells lining the proximal and distal borders of each annulus. These high density zones were observed as early as two hr. a.p., and expanded with mitotic activity to fill the mid-annular regions by about 72 hrs a.p. Mitotic activity initiated at a low rate, increasing dramatically after 40-48 hrs a.p.; this activity was enhanced by ecdysteroids, but did not occur in animals entering pupal diapause (which is also ecdysteroid sensitive).Conclusions/significanceSensory proliferation initiates in narrow zones along the proximal and distal borders of each annulus; these zones rapidly expand to fill the mid-annular regions. These zones exist prior to any mitotic activity as regions of high density cells which form either at or prior to pupation. Mitotic sensitivity to ecdysteroids may be a regulatory mechanism coordinating olfactory development with the developmental choice of diapause entry.

Dataset Information

Biological Mechanisms for Learning: A Computational Model of Olfactory Learning in the Manduca sexta Moth, With Applications to Neural Nets.

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