The Frequency Preference of Neurons and Synapses in a Recurrent Oscillatory Network

Abstract

A variety of neurons and synapses shows a maximal response at a preferred frequency, generally considered to be important in shaping network activity. We are interested in whether all neurons and synapses in a recurrent oscillatory network can have preferred frequencies and, if so, whether these frequencies are the same or correlated, and whether they influence the network activity. We address this question using identified neurons in the pyloric network of the crab Cancer borealis. Previous work has shown that the pyloric pacemaker neurons exhibit membrane potential resonance whose resonance frequency is correlated with the network frequency. The follower lateral pyloric (LP) neuron makes reciprocally inhibitory synapses with the pacemakers. We find that LP shows resonance at a higher frequency than the pacemakers and the network frequency falls between the two. We also find that the reciprocal synapses between the pacemakers and LP have preferred frequencies but at significantly lower values. The preferred frequency of the LP to pacemaker synapse is correlated with the presynaptic preferred frequency, which is most pronounced when the peak voltage of the LP waveform is within the dynamic range of the synaptic activation curve and a shift in the activation curve by the modulatory neuropeptide proctolin shifts the frequency preference. Proctolin also changes the power of the LP neuron resonance without significantly changing the resonance frequency. These results indicate that different neuron types and synapses in a network may have distinct preferred frequencies, which are subject to neuromodulation and may interact to shape network oscillations.

Short-Term Synaptic Dynamics Control the Activity Phase of Neurons in an Oscillatory Network

“…For a given synaptic duration T act , the peak phase of the synapse can be defined as Δ peak = t peak / T act ). The parameter Δ peak is known to vary as a function of P (Tseng et al, 2014) and, in a previous study, we found that Δ peak may influence the activity of the postsynaptic neuron, independent of P and g max (Mamiya and Nadim, 2004). We therefore systematically explored the influence of three parameters of the synaptic input ( P, g max and Δ peak ) on φ LP .…”

“…The case is less clear for the finding that an increase of Δ peak with P promotes phase maintenance, as we have previously shown that Δ peak in LP actually decreases with P (Manor et al, 1997; Tseng et al, 2014). On the face of it, this suggests that an increase in Δ peak is not a strategy employed in the intact circuit.…”

Neuromodulation of astrocytic K+ clearance

“…Parkinson's disease, Alzheimer's disease, schizophrenia, depression) (Panula et al, 1997;Ray et al, 2008;Heneka et al, 2010). At the cellular level, synaptic release of neuromodulators impact membrane properties as well as intracellular signalling pathways in both neurons and glial cells Ma et al, 2016), and previous reports showed that different neuromodulators can fine-tune the hyperpolarization-activated current Ih (Maccaferri & McBain, 1996;Rosenkranz, 2006;Ma et al, 2007), thereby affecting membrane resonance of individual neurons, which affect the oscillatory behaviour of single neurons and their synchronization into networks (Tseng et al, 2014). However, whether this was a direct effect of the neuromodulators on neuronal activity, or indirect via astrocytic modulation was never tested.…”

The complexity of small circuits: the stomatogastric nervous system

“…show best responses at specific input frequencies. The distinct frequency preferences of different network components are correlated with the period of the rhythm and potentially the phasing of neurons, and are altered when neuromodulators change circuit activity [15*]. …”