Gamma oscillations mediate stimulus competition and attentional selection in a cortical network model

Abstract

Simultaneous presentation of multiple stimuli can reduce the firing rates of neurons in extrastriate visual cortex below the rate elicited by a single preferred stimulus. We describe computational results suggesting how this remarkable effect may arise from strong excitatory drive to a substantial local population of fast-spiking inhibitory interneurons, which can lead to a loss of coherence in that population and thereby raise the effectiveness of inhibition. We propose that in attentional states fast-spiking interneurons may be subject to a bath of inhibition resulting from cholinergic activation of a second class of inhibitory interneurons, restoring conditions needed for gamma rhythmicity. Oscillations and coherence are emergent features, not assumptions, in our model. The gamma oscillations in turn support stimulus competition. The mechanism is a form of ''oscillatory selection,'' in which neural interactions change phase relationships that regulate firing rates, and attention shapes those neural interactions.cholinergic modulation ͉ selective attention ͉ gamma rhythm C ortical gamma frequency (30-90 Hz) oscillations are known to be associated with many aspects of cognition, including sensory processing, attention, memory, and awareness (1). However, the biophysical underpinnings of gamma oscillations and the means by which they contribute to cognitive processing are still not fully understood. Here we continue a series of computational studies investigating how the biophysics of the gamma rhythm, and in particular its neuromodulation, affect network processing associated with attention (2-4).We focus on the much-cited experiments of Desimone and colleagues (5-7). These showed that orientation-selective principal neurons in macaque V2 and V4 respond to simultaneous presentation of preferred (''good'') and nonpreferred (''poor'') stimuli in their receptive fields at spike rates well below those elicited by the preferred stimulus alone. Furthermore, when attention is directed to either of the two stimuli, the neuron responds almost as if the unattended stimulus were absent.The essence of the mechanism we propose here is a relationship between the effectiveness of the excitatory inputs to the target network and the coherence of the network's inhibitory cells: The same drive that produces a robust response when the inhibition is coherent produces a much less robust response when the inhibition is incoherent. We describe how this mechanism can, qualitatively at least, explain the results in (5-7).Selective attention is associated with an increase in coherence of spiking and in spectral power of oscillations in the gamma frequency band (8-10). The model we offer here does not assume a priori that bottom-up or top-down input is made more coherent or more oscillatory as a result of attention (11,12). Rather, the increased gamma power and coherence of the network output are consequences of the biophysical effects of cholinergic modulation. A critical feature of the model is that the target entity of competing stream...

Cognitive fitness of cost-efficient brain functional networks

“…This is compatible with the interpretation that maximization of cost efficiency in the highest-frequency ␥-network may be affiliated more strongly with attentional components and less directly with memory performance. Indeed, there is strong evidence to suggest that the ␥-band is important as a physiological substrate for sensorimotor binding and may more specifically mediate attentional selection (29,30).…”

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

“…3D). In this sense, there is no competition between the original cells receiving stimulation (RS1) and the new ones (RS2); unlike the situation of PING gamma (7,14), the introduction of another and larger input to a subset of pyramidal cells (RS2) does not suppress the RS1 activity.…”

“…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).…”

“…Second, there is enormous overlap in the axonal fields of FS interneurons and a great deal of convergence and divergence of inhibition in the PING circuit (12, 13). It follows that, if two subsets of cells are given enough excitation to form cell assemblies and one is given more than the other, the cells receiving the lower amount of excitation can be suppressed (7,14). The cells with the highest excitation determine the frequency of the inhibitory cells and cause them to fire faster than if they were interacting with the less excited group of cells.…”

“…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)(8)(9)(10)(11). In this rhythm, activated pyramidal cells excite fast-spiking perisomatictargeting interneurons (FS cells) that, in turn, inhibit the pyramidal cells; the period of the oscillation corresponds to the time necessary for the inhibition to decay and allow the pyramidal cells to spike once again.…”