Abstract
Connections between neuronal populations may be genetically hardwired or random. In the insect olfactory system, projection neurons of the antennal lobe connect randomly to Kenyon cells of the mushroom body. Consequently, while the odor responses of the projection neurons are stereotyped across individuals, the responses of the Kenyon cells are variable. Surprisingly, downstream of Kenyon cells, mushroom body output neurons show stereotypy in their responses. We found that the stereotypy is enabled by the convergence of inputs from many Kenyon cells onto an output neuron, and does not require learning. The stereotypy emerges in the total response of the Kenyon cell population using multiple odor-specific features of the projection neuron responses, benefits from the nonlinearity in the transfer function, depends on the convergence:randomness ratio, and is constrained by sparseness. Together, our results reveal the fundamental mechanisms and constraints with which convergence enables stereotypy in sensory responses despite random connectivity.
Highlights
Connections between neuronal populations may be genetically hardwired or random
Hige et al.[20] measured the odor responses of identified mushroom body output neurons (MBONs) in different flies and found that MBONs responses across individuals were not identical but many of the MBONs had significantly more correlations across individuals than expected by chance. How do these MBONs generate stereotypic responses, when their input comes from Kenyon cells (KCs) with non-stereotypic responses? mushroom bodies have been traditionally viewed as responsible for learning and memory, recent studies show that some MBONs are involved in innate behaviors[21,22,23], and consistent responses across animals for untrained stimuli are desirable
As stereotypy has been examined in only Drosophila MBONs so far[20], we first checked whether MBONs in other species have stereotypic responses
Summary
In the insect olfactory system, projection neurons of the antennal lobe connect randomly to Kenyon cells of the mushroom body. While the odor responses of the projection neurons are stereotyped across individuals, the responses of the Kenyon cells are variable. Hige et al.[20] measured the odor responses of identified MBONs in different flies and found that MBONs responses across individuals were not identical but many of the MBONs had significantly more correlations across individuals than expected by chance How do these MBONs generate stereotypic responses, when their input comes from KCs with non-stereotypic responses? We show that stereotypy is a natural consequence of convergence following random connectivity and does not require learning These observations from simulations are confirmed by deriving a closed-form expression for stereotypy in an analytical model. Our results reveal the fundamental mechanisms and constraints that determine the level of stereotypy in any neural network with random connections
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