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.

Fig. 1.

Cartoon representation of the components in the computational model. (A) The computational model consists of two layers. The superficial layer gamma model consists of two interconnected cells types: regular spiking (RS) pyramidal cells and basket (b) cells, all modeled as single compartments. The deep layer beta2 model consists of intrinsically bursting (IB) cells modeled with four compartments (an apical dendrite, a basal dendrite, a soma, and an axon labeled d_a, d_b, IB, and a, respectively). The superficial layer also contains single compartment models of low-threshold spiking (LTS) interneurons. Excitatory synaptic connections are represented as solid lines. Each RS cell connects to all basket cells, all LTS cells, and three IB cells. Each IB cell connects to all basket and LTS cells. Inhibitory connections are represented as dashed lines. Each basket cell connects to itself, one LTS interneuron, and all RS cells. Each LTS interneuron connects to itself, four RS cells, and one IB cell. (B) Example of superficial layer gamma activity and deep layer beta2 activity. Each basket cell spikes on nearly every cycle of the gamma rhythm, whereas the RS cells (divided into two populations) spike more sparsely. The deep layer IB cells burst at beta2 frequency. (C) Histogram showing the number of spikes per second generated by RS cells when both populations are activated simultaneously (resulting in competition), and when activated independently. During competition, the RS2 assembly generates less spikes per second than when activated independently (i.e., when RS1 is not activated). During competition, the more active RS1 assembly suppresses the RS2 assembly, decreasing its firing rate by 8 Hz. In this histogram, and all histograms that follow, we summarize the results of 10 simulation realizations, each with different initial conditions and realizations of stochastic input.

Fig. 2.

Model population dynamics during intervals of high and low excitation reveal different neural rhythms. (A) Cartoon representation of stimulus presentation to the model. In the first interval (label 1st), both superficial layer RS assemblies receive increased excitatory drive. RS1 (upper curve) receives more drive than RS2 (lower curve), representing in the model responses to an unfamiliar stimulus by RS1 and familiar stimulus by RS2. In the second interval (label 2nd), the excitatory drive from the unfamiliar stimulus to RS1 has decayed slowly, whereas the drive from the familiar stimulus to RS2 has decayed rapidly. (B) Example rastergram resulting during the first stimulus presentation. The superficial layer basket and RS cells generate a gamma oscillation, whereas the deep layer IB cells generate a beta2 rhythm. (C) Histogram of the RS1 (Upper) and RS2 (Lower) activity as a function of beta2 phase. No phase relationship exists between the superficial layer and deep layer cells. (D) Example rastergram during the second stimulus presentation. Now the superficial and deep layer cells coordinate to generate a beta1 rhythm. The excitatory drive to the RS2 cells decays sufficiently so that these cells rarely participate in the beta1 rhythm. (E) Histograms of the RS1 and RS2 activity reveal that the RS1 cells generate spikes at a particular phase of beta1.

Fig. 3.

Reactivation of cells by a familiar input nests superficial layer gamma activity within the beta1 rhythm. (A) In the second interval, the familiar input reactivates cell assembly RS2; this reactivation provides 80% of the excitatory drive delivered in the first interval. (B) Example rastergram during reactivation shows RS2 and RS1 become more active, now spiking twice during each beta1 cycle. (C) Histograms for RS1 (Upper) and RS2 (Lower) during reactivation indicate the two beta1 phases at which the superficial layer RS cells spike—once near 130 degrees, and once just before the deep layer IB cells burst. (D) Histogram of the number of RS1 spikes that appear out of phase with the beta1 rhythm (i.e., in phase bins ≥120 degrees and ≤−150 degrees) during the baseline beta1 condition (as in Fig. 2D) and during reactivation of RS2 (as in this figure). The RS1 assembly generates approximately the same number of spikes in the out-of-phase interval whether or not the RS2 cells receive the additional, familiar stimulus. (E and F) Example rastergram and histogram for model dynamics identical to B and C but including all-to-all synaptic connections between the pyramidal cells in RS1. Inclusion of these synapses has little impact on the observed dynamics.

Fig. 4.

Reactivation of cells by inputs nests superficial layer gamma activity within the beta1 rhythm. (A) In the second interval, inputs reactivate cell assemblies RS1 and RS2. (B) Example rastergram during reactivation shows RS2 and RS1 become more active, now spiking two or three times during each beta1 cycle. (C) Histograms for RS1 (Upper) and RS2 (Lower) during reactivation indicate the beta1 phases at which the superficial layer RS cells spike. Both assemblies generate spikes near ±120 degrees, and RS1 also spikes near 0 degrees. (D and E) Example rastergram and histogram for model dynamics identical to B and C but including all-to-all synaptic connections between the pyramidal cells in RS1. Inclusion of these synapses has little impact on the observed dynamics. (F) Histogram showing the number of spikes per second generated by RS cells when both populations are reactivated simultaneously (Left) and when reactivated independently (Right). Both assemblies generate approximately the same number of spikes per second when activated simultaneously (as in this figure) or independently (as in Fig. 3 for RS2). (G) The competition ratio is the number of spikes generated by RS2 when activated simultaneously with RS1 versus when activated independently. In the first presentation of the stimulus, the RS2 assembly generates fewer spikes when activated simultaneously with RS1. In the second presentation, RS2 generates nearly the same number of spikes whether or not RS1 is simultaneously activated.