Common excitatory input to neurons increases their firing rates and the strength of the spike correlation (synchrony) between them. Little is known, however, about the synchronizing effects of modulatory common input. Here, we show that modulatory common input with the slow synaptic kinetics of N-methyl-d-aspartate (NMDA) receptors enhances firing rates and also produces synchrony. Tight synchrony (correlations on the order of milliseconds) always increases with modulatory strength. Unexpectedly, the relationship between strength of modulation and strength of loose synchrony (tens of milliseconds) is not monotonic: The strongest loose synchrony is obtained for intermediate modulatory amplitudes. This finding explains recent neurophysiological results showing that in cortical areas V1 and V2, presumed modulatory top-down input due to contour grouping increases (loose and tight) synchrony but that additional modulatory input due to top-down attention does not change tight synchrony and actually decreases loose synchrony. These neurophysiological findings are understood from our model of integrate-and-fire neurons under the assumption that contour grouping as well as attention lead to additive modulatory common input through NMDA-type synapses. In contrast, circuits with common projections through model α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors did not exhibit the paradoxical decrease of synchrony with increased input. Our results suggest that NMDA receptors play a critical role in top-down response modulation in the visual cortex.
Directing attention to the spatial location or the distinguishing feature of a visual object modulates neuronal responses in the visual cortex and the stimulus discriminability of subjects. However, the spatial and feature-based modes of attention differently influence visual processing by changing the tuning properties of neurons. Intriguingly, neurons' tuning curves are modulated similarly across different visual areas under both these modes of attention. Here, we explored the mechanism underlying the effects of these two modes of visual attention on the orientation selectivity of visual cortical neurons. To do this, we developed a layered microcircuit model. This model describes multiple orientation-specific microcircuits sharing their receptive fields and consisting of layers 2/3, 4, 5, and 6. These microcircuits represent a functional grouping of cortical neurons and mutually interact via lateral inhibition and excitatory connections between groups with similar selectivity. The individual microcircuits receive bottom-up visual stimuli and top-down attention in different layers. A crucial assumption of the model is that feature-based attention activates orientation-specific microcircuits for the relevant feature selectively, whereas spatial attention activates all microcircuits homogeneously, irrespective of their orientation selectivity. Consequently, our model simultaneously accounts for the multiplicative scaling of neuronal responses in spatial attention and the additive modulations of orientation tuning curves in feature-based attention, which have been observed widely in various visual cortical areas. Simulations of the model predict contrasting differences between excitatory and inhibitory neurons in the two modes of attentional modulations. Furthermore, the model replicates the modulation of the psychophysical discriminability of visual stimuli in the presence of external noise. Our layered model with a biologically suggested laminar structure describes the basic circuit mechanism underlying the attention-mode specific modulations of neuronal responses and visual perception.
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