Top-down beta rhythms support selective attention via interlaminar interaction: a model

Abstract

Cortical rhythms have been thought to play crucial roles in our cognitive abilities. Rhythmic activity in the beta frequency band, around 20 Hz, has been reported in recent studies that focused on neural correlates of attention, indicating that top-down beta rhythms, generated in higher cognitive areas and delivered to earlier sensory areas, can support attentional gain modulation. To elucidate functional roles of beta rhythms and underlying mechanisms, we built a computational model of sensory cortical areas. Our simulation results show that top-down beta rhythms can activate ascending synaptic projections from L5 to L4 and L2/3, responsible for biased competition in superficial layers. In the simulation, slow-inhibitory interneurons are shown to resonate to the 20 Hz input and modulate the activity in superficial layers in an attention-related manner. The predicted critical roles of these cells in attentional gain provide a potential mechanism by which cholinergic drive can support selective attention.

Figure 1. The structure of the model.

(A). Structure of a single column. Each circle is a population of 20 cells. Open and solid arrows represent NMDA and AMPA synapses respectively. Blue circles are GABA synapses. (B). Full model. Two columns interact with each other via ascending excitatory synapses from L5 pyramidal cells to L2/3 FS and SI cells. Both columns receive 100 Hz Poisson EPSC trains. Synchronous top-down signals are introduced into the attended column only. For clarity, we do not display recurrent connections inside the population of the same type: all cells interact with others that belong to the same population (see Methods).

Figure 2. Cell activity in response to top-down beta rhythms.

(A)–(I). Neural responses of the control (without bottom-up or top-down inputs), attended and the unattended columns. Each dot represents an action potential. x-axis shows simulation time, and y-axis displays the cell number.

Figure 3. The effect of top-down beta rhythms on neural responses.

(A). The power spectra of STA of LFPs in all three conditions. (B). The average firing rate of L2/3 RS cells from 10 simulations, and the error bar is the standard deviation of 10 simulations. (C). Scatter plots of attentional indices; AI(R) on x-axis, AI(/) on y-axis.

Figure 4. The effect of top-down beta rhythms on neural responses without L2/3 SI cells.

All parameters are the same as in Figure 3, but with SI cells removed from the network. (A). The firing rate of L2/3 RS cell activity from 10 simulation. (B). The power spectra of STA of LFPs.

Figure 5. Neural activity during the stimulus period.

(A)–(I). Neural responses of the control, attended and the attended columns, respectively.

Figure 6. The effect of top-down beta rhythms on neural responses during the stimulus period.

(A). The firing rate of L2/3 RS cells. (B). The power spectra of STA of LFPs. A logarithmic scale is used on y-axis. (C)–(D). Scatter plots of attentional indices.

Figure 7. Functional roles of ascending inhibition.

(A). The power spectra of STA of LFPs in the attended and unattended columns, without ascending inhibition from L5 SI cells to L4 FS cells. (B). Comparison of AI(), with and without ascending inhibition. (C). Difference in average membrane potentials between L4 E and L4 FS cells, , where is the mean value of membrane potentials over 20 cells. Thus, positive peaks represent moments when more L4 E cells spike than L4 FS cells, and negative peaks show moments when more L4 FS cells spike more than L4 E cells. The membrane potential difference in the attended column is compared, with and without ascending inhibition. (D). Comparison of the firing rate of L4 E cells of the attended column, with and without ascending inhibition. (E). Comparison of between the attended and unattended columns with ascending inhibition. (F). Comparison of the firing rate of L4 E cells between the attended and unattended columns.

Figure 8. The impact of intercolumnar connections on attentional modulation.

Attentional indices with gradually reduced intercolumbar projection. AI(/), AI(), AI(R) are displayed in (A),(B) and (C), respectively. * represents distributions significantly different from 0.

Figure 9. Functional roles of L2/3 SI cells.

(A)–(B). Superficial activity without L2/3 SI cells. (C). The firing rate of L2/3 RS cells, with and without L2/3 SI cells. (D)–(E). Comparison of attentional indices, with and without L2/3 SI cells. For each index, bar graphs show mean values from 10 simulations, and errorbars are standard errors from 10 simulations. (F). Comparison of the synchrony in RS cell activity, with and without L2/3 SI cells.

Figure 10. The effect of excitability of FS cells.

Comparison of attentional indices. (A). The effect on the synchrony in the gamma frequency band. (B). The effect on the firing rate of L2/3 RS cells. * represents distributions significantly different from 0.

Figure 11. The effect of asynchronous top-down signals.

(A). The power spectra of STA of LFPs with asynchronous top-down signals. (B). Attentional indices; all indices are not significantly different from 0. (C)–(H). Cell activity in both columns with asynchronous top-down signals.