Neuronal assembly dynamics in the beta1 frequency range permits short-term memory

Abstract

Cell assemblies have long been thought to be associated with brain rhythms, notably the gamma rhythm. Here, we use a computational model to show that the beta1 frequency band, as found in rat association cortex, has properties complementary to the gamma band for the creation and manipulation of cell assemblies. We focus on the ability of the beta1 rhythm to respond differently to familiar and novel stimuli, and to provide a framework for combining the two. Simulations predict that assemblies of superficial layer pyramidal cells can be maintained in the absence of continuing input or synaptic plasticity. Instead, the formation of these assemblies relies on the nesting of activity within a beta1 rhythm. In addition, cells receiving further input after assembly formation produce coexistent spiking activity, unlike the competitive spiking activity characteristic of assembly formation with gamma rhythms.postinhibitory rebound | synchrony I t has been highly documented that rhythms of the central nervous system are associated with cognition (1). However, the ways in which brain rhythms are important to cognitive function are not well understood. One suggested function for rhythms has been the creation of cell assemblies (collections of neurons that are transiently synchronous). The rhythm most associated with the formation of such cell assemblies is the gamma frequency band (30-90 Hz) (2-4). Other rhythms, however, may play an important role in the formation or transformation of cell assemblies. Here, we build on experimental and modeling work concerning the beta1 frequency band (≈15 Hz), as found in rat association cortex (5, 6), to show that this version of the beta1 rhythm has special physiological properties appropriate to manipulation of cell assemblies. We are especially interested here in how networks producing this rhythm respond to familiar and novel stimuli and how the underlying physiology provides a context for combining the two. A key feature of the model given below is that the spiking during beta1 depends on rebound from inhibition, allowing activity to be maintained in the absence of continuing input. The "memory"-provided by the ability to have ongoing activity-is independent of synaptic plasticity. The model also shows that the nesting of gamma activity inside the beta1 oscillation produces different interactions of cell assemblies than in the absence of the beta1 rhythm: There is much less of the competition characteristic of cell assemblies produced within the gamma rhythm (7).To appreciate the novel features of cell assemblies formed within the beta1 rhythm, it is necessary to understand some central features of the gamma rhythm and its assembly-forming properties. The type of gamma rhythm associated with cell assemblies is known as the pyramidal interneuron network gamma (or PING) rhythm (4). This kind of gamma is produced mainly by pyramidal cells and fast-spiking interneurons (7-11). In this rhythm, activated pyramidal cells excite fast-spiking perisomatictargeting interneurons (FS cells) that,...

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