Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts

Odour representations in insects undergo progressive transformations and decorrelatio from the receptor array to the presumed site of odour learning, the mushroom body. There, odours are represented by sparse assemblies of Kenyon cells in a large population. Using intracellular recordings in vivo, we examined transmission and plasticity at the synapse made by Kenyon cells onto downstream targets in locusts. We find that these individual synapses are excitatory and undergo hebbian spike-timing dependent plasticity (STDP) on a ±25 ms timescale. When placed in the context of odour-evoked Kenyon cell activity (a 20-Hz oscillatory population discharge), this form of STDP enhances the synchronization of the Kenyon cells’ targets and thus helps preserve the propagation of the odour-specific codes through the olfactory system

Neural Encoding of Odors during Active Sampling and in Turbulent Plumes

Sensory inputs are often fluctuating and intermittent, yet animals reliably utilize them to direct behavior. Here we ask how natural stimulus fluctuations influence the dynamic neural encoding of odors. Using the locust olfactory system, we isolated two main causes of odor intermittency: chaotic odor plumes and active sampling behaviors. Despite their irregularity, chaotic odor plumes still drove dynamic neural response features including the synchronization, temporal patterning, and short-term plasticity of spiking in projection neurons, enabling classifier-based stimulus identification and activating downstream decoders (Kenyon cells). Locusts can also impose odor intermittency through active sampling movements with their unrestrained antennae. Odors triggered immediate, spatially targeted antennal scanning that, paradoxically, weakened individual neural responses. However, these frequent but weaker responses were highly informative about stimulus location. Thus, not only are odor-elicited dynamic neural responses compatible with natural stimulus fluctuations and important for stimulus identification, but locusts actively increase intermittency, possibly to improve stimulus localization

Spike-Timing Dependent Plasticity and Synchronous Oscillations in an Invertebrate Olfactory System

Sensory systems neuroscience aims to study how patterns of neural activity represent stimuli of the outside world. To this end, the present work addresses how olfactory stimuli are represented by three successive layers in the locust olfactory system. Activation by an odorant of primary sensory neurons in the antenna gives rise to broadly distributed, oscillatory spatiotemporal activity patterns across the antennal lobe (AL). This is in marked contrast to the representation in the mushroom body (MB), where Kenyon cells (KCs) respond very sparsely and very briefly. In the AL, an odor gives rise to a particular trajectory through Projection Neuron (PN) phase space, with individual timepoints representing different aspects of the stimulus; in the MB, very small subsets of KCs respond selectively at particular timepoints along this trajectory. Two mechanisms are identified that contribute to the sparsening across the two structures: an intrinsic voltage dependence in the KCs, which gives rise to a superlinear response to synchronous inputs, and a canonical network motif, feedforward inhibition, which diminishes the KC response to nonsynchronous excitatory inputs. From a decoding perspective, this makes the oscillation cycle the relevant timestep of the AL trajectories, and it demonstrates a role for synchronous oscillations in sensory networks. While broad activation of the AL promotes extensive local interactions, giving rise to dynamic representations and enabling multiple features to be extracted, the sparse representation after decoding by KCs likely facilitates the storage of relevant patterns in memory. A subset of MB extrinsic neurons with dendrites densely invading the β-lobe (βLNs) is well placed to decode the KCs’ sparse responses. The synapses formed by KCs onto these cells are powerful and undergo Hebbian spike-timing dependent plasticity (STDP) on a timescale similar to the synchronous oscillations generated in the AL (and propagated through the MB). STDP has a homeostatic effect on the firing phase of βLNs by fine-tuning the strength of KC-βLN synapses, contributing to tight locking among subsets of βLNs during odor stimulation and facilitating the flow of synchronous information. The facilitation of tight synchrony among βLNs by STDP further ensures that different odor features computed and formatted as a function of cycle number by the AL, and represented by the sparse representations of KCs, remain segregated between LFP oscillation cycles. This segregation is also sustained by phase locked feedforward inhibition onto βLNs, which restricts the window of integration for inputs from KCs, and is found to be due to neighboring βLNs of the same class. The implications of the resultant competition among βLNs due to this inhibition, and particularly its interaction with STDP at the KC-βLN synapse are addressed with a network model. The results are considered within the context of the circuit in which the KC-βLN network is embedded, and a cycle-specific mechanism for learning an arbitrary subset of the odor features computed in the AL is proposed.</p

Conditional modulation of spike-timing-dependent plasticity for olfactory learning

Mushroom bodies are a well-known site for associative learning in insects. Yet the precise mechanisms that underlie plasticity there and ensure their specificity remain elusive. In locusts, the synapses between the intrinsic mushroom body neurons and their postsynaptic targets obey a Hebbian spike-timing-dependent plasticity (STDP) rule. Although this property homeostatically regulates the timing of mushroom body output, its potential role in associative learning is unknown. Here we show in vivo that pre–post pairing causing STDP can, when followed by the local delivery of a reinforcement-mediating neuromodulator, specify the synapses that will undergo an associative change. At these synapses, and there only, the change is a transformation of the STDP rule itself. These results illustrate the multiple actions of STDP, including a role in associative learning, despite potential temporal dissociation between the pairings that specify synaptic modification and the delivery of reinforcement-mediating neuromodulator signals

Oscillations and sparsening of odor representations in the mushroom body

In the insect olfactory system, oscillatory synchronization is functionally relevant and reflects the coherent activation of dynamic neural assemblies. We examined the role of such oscillatory synchronization in information transfer between networks in this system. The antennal lobe is the obligatory relay for olfactory afferent signals and generates oscillatory output. The mushroom body is responsible for formation and retrieval of olfactory and other memories. The format of odor representations differs significantly across these structures. Whereas representations are dense, dynamic, and seemingly redundant in the antennal lobe, they are sparse and carried by more selective neurons in the mushroom body. This transformation relies on a combination of oscillatory dynamics and intrinsic and circuit properties that act together to selectively filter and synthesize the output from the antennal lobe. These results provide direct support for the functional relevance of correlation codes and shed some light on the role of oscillatory synchronization in sensory networks. Electroencephalogram and local field potentia