Inhibitory synchrony as a mechanism for attentional gain modulation

Abstract

Recordings from area V4 of monkeys have revealed that when the focus of attention is on a visual stimulus within the receptive field of a cortical neuron, two distinct changes can occur: The firing rate of the neuron can change and there can be an increase in the coherence between spikes and the local field potential (LFP) in the gamma-frequency range (30-50 Hz). The hypothesis explored here is that these observed effects of attention could be a consequence of changes in the synchrony of local interneuron networks. We performed computer simulations of a Hodgkin-Huxley type neuron driven by a constant depolarizing current, I, representing visual stimulation and a modulatory inhibitory input representing the effects of attention via local interneuron networks. We observed that the neuronÕs firing rate and the coherence of its output spike train with the synaptic inputs was modulated by the degree of synchrony of the inhibitory inputs. When inhibitory synchrony increased, the coherence of spiking model neurons with the synaptic input increased, but the firing rate either increased or remained the same. The mean number of synchronous inhibitory inputs was a key determinant of the shape of the firing rate versus current (f-I) curves. For a large number of inhibitory inputs ($50), the f-I curve saturated for large I and an increase in input synchrony resulted in a shift of sensitivity-the model neuron responded to weaker inputs I. For a small number ($10), the f-I curves were non-saturating and an increase in input synchrony led to an increase in the gain of the response-the firing rate in response to the same input was multiplied by an approximately constant factor. The firing rate modulation with inhibitory synchrony was highest when the input network oscillated in the gamma frequency range. Thus, the observed changes in firing rate and coherence of neurons in the visual cortex could be controlled by top-down inputs that regulated the coherence in the activity of a local inhibitory network discharging at gamma frequencies.

Regulation of spike timing in visual cortical circuits

“…This reduces the firing rate of the remaining interneurons and synchronizes the 'winners'. Recent modelling work advanced the hypothesis that the effects of selective attention are mediated by the top-down activation of interneurons [116][117][118][119][120][121] . Taken together, the different aspects of this model 115 predict that selective attention strongly increases the firing rate of a subset of inhibitory neurons; this was recently confirmed experimentally 122 .…”

“…In the model, a change in interneuron synchrony could affect the postsynaptic neuron in two ways 116 . The first is by a process called multiplicative gain (FIG.…”

“…Multiplicative-gain modulation is important because it increases or decreases the overall strength of the neuron's response while preserving the stimulus preference of the neuron 124 . The timescale of the inhibitory conductance is such that this modulation is better achieved for oscillations in the gamma frequency range 116 . Second, changes in interneuron synchrony could act as a gate, preventing spiking when the network is asynchronous and allowing spiking when the network is synchronous.…”

“…The value of the jitter for each curve, expressed in milliseconds, is shown in the key. The data were obtained from simulations of a singlecompartment model 116 . e| An example of selective communication using phase relationships.…”

Anticipation of natural stimuli modulates EEG dynamics: physiology and simulation

“…The noise that comes with such balanced input has recently been shown to account for contrast normalization in the primary visual cortex of cats (Finn et al 2007). A second mechanism that could implement gain modulation is synchrony of inhibitory cells (Tiesinga et al 2004). Cells that receive highly synchronous inhibitory input appear to have a higher input gain than cells for which the inhibitory input is temporally uncorrelated.…”