Sub-threshold oscillations are ubiquitous throughout the brain and span wide range frequencies. While the sources of these oscillations are not well understood, they are known to originate from various brain regions, and thus have different cognitive function depending on their spectral properties
[1]. Some of these oscillations maybe generated by intrinsic neural oscillators, others are thought to originate from network interactions. For example, theta rhythms (6–10 Hz) originate in hippocampus and have been shown to correspond to the ‘active learning’ state
[2],
[3]. Theta rhythms have been implicated in learning and the encoding of memories
[4]–
[6]. These oscillations, along with synaptic modification via spike-timing-dependent plasticity (STDP) provide the necessary basis for the formation and changes of memory traces in neuronal networks of the brain
[6]–
[8]. At the same time, cortico-cortical and thalamocortical networks are implicated in generation of alpha rhythms (8–12 Hz)
[9], while beta rhythms are mostly generated in motor cortex. Gamma rhythms (20–80 Hz) are widely distributed over the cortex and are thought to be mediated by fast-spiking inhibitory interneurons. Their function is still not well understood but one possible implication is in controlling sensory responses
[10].
At the same time it has been demonstrated that certain types of neurons have the ability to resonate
[11],
[12] and fire in response to a specific sub-threshold oscillatory current. Furthermore, it has also been recently shown that this natural frequency can shift in response to changes in the neuron's membrane potential
[13],
[14]. Here we propose a novel mechanism linking these three experimentally observed phenomena in which a neuronal network may utilize intrinsic oscillatory patterning, together with cell's ability to resonate and dynamically shift its resonant frequency, as a means to encode patterns based on the characteristics of a
sub-threshold signal current. We show that changing the magnitude of the sub-threshold input can shift the cells' natural frequency into, and out of, the sub-threshold oscillatory current's range. This causes the neuron to resonate and phase lock to the period of the oscillation when the signal current is within a certain range. We use a network of resonate-and-fire (RAF)
[15] neurons to demonstrate that this mechanism generates a highly selective spatio-temporal firing pattern. We compare the response properties of this network to a supra-threshold stimulated RAF network and to a network of supra-threshold stimulated integrate and fire neurons (IAF), all receiving sub-threshold oscillatory currents. We show that the RAF frequency adaptation mechanism is far superior at resolving temporal correlations/differences than the other models. This property, in conjunction with spike timing dependent plasticity (STDP), can be utilized to store temporal correlations between different input. Finally, we use this natural frequency shift mechanism to explain two experimentally observed phenomena in the hippocampus: the phase precession
[16],
[17] along theta oscillation observed in the firing of hippocampal place cells as animal traverses its place field, and the dynamic changes in phase locking observed between the medial prefrontal cortex and the ventral or dorsal hippocampus during fear or a working memory task respectively
[18],
[19].
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