A single GABAergic neuron mediates feedback of odor-evoked signals in the mushroom body of larval Drosophila

Front Neural Circuits. 2014 Apr 9;8:35. doi: 10.3389/fncir.2014.00035. eCollection 2014.

Abstract

Inhibition has a central role in defining the selectivity of the responses of higher order neurons to sensory stimuli. However, the circuit mechanisms of regulation of these responses by inhibitory neurons are still unclear. In Drosophila, the mushroom bodies (MBs) are necessary for olfactory memory, and by implication for the selectivity of learned responses to specific odors. To understand the circuitry of inhibition in the calyx (the input dendritic region) of the MBs, and its relationship with MB excitatory activity, we used the simple anatomy of the Drosophila larval olfactory system to identify any inhibitory inputs that could contribute to the selectivity of MB odor responses. We found that a single neuron accounts for all detectable GABA innervation in the calyx of the MBs, and that this neuron has pre-synaptic terminals in the calyx and post-synaptic branches in the MB lobes (output axonal area). We call this neuron the larval anterior paired lateral (APL) neuron, because of its similarity to the previously described adult APL neuron. Reconstitution of GFP partners (GRASP) suggests that the larval APL makes extensive contacts with the MB intrinsic neurons, Kenyon Cells (KCs), but few contacts with incoming projection neurons (PNs). Using calcium imaging of neuronal activity in live larvae, we show that the larval APL responds to odors, in a manner that requires output from KCs. Our data suggest that the larval APL is the sole GABAergic neuron that innervates the MB input region and carries inhibitory feedback from the MB output region, consistent with a role in modulating the olfactory selectivity of MB neurons.

Keywords: APL neuron; inhibition; mushroom body calyx; odor discrimination; olfaction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Discrimination, Psychological / physiology
  • Drosophila / physiology
  • GABAergic Neurons / physiology*
  • Larva / physiology*
  • Learning / physiology
  • Memory / physiology
  • Mushroom Bodies / physiology*
  • Odorants*
  • Olfactory Perception / physiology*
  • Smell / physiology*