Routing information flow by separate neural synchrony frequencies allows for “functionally labeled lines” in higher primate cortex

Abstract

Efficient transfer of sensory information to higher (motor or associative) areas in primate visual cortical areas is crucial for transforming sensory input into behavioral actions. Dynamically increasing the level of coordination between single neurons has been suggested as an important contributor to this efficiency. We propose that differences between the functional coordination in different visual pathways might be used to unambiguously identify the source of input to the higher areas, ensuring a proper routing of the information flow. Here we determined the level of coordination between neurons in area MT in macaque visual cortex in a visual attention task via the strength of synchronization between the neurons’ spike timing relative to the phase of oscillatory activities in local field potentials. In contrast to reports on the ventral visual pathway, we observed the synchrony of spikes only in the range of high gamma (180 to 220 Hz), rather than gamma (40 to 70 Hz) (as reported previously) to predict the animal’s reaction speed. This supports a mechanistic role of the phase of high-gamma oscillatory activity in dynamically modulating the efficiency of neuronal information transfer. In addition, for inputs to higher cortical areas converging from the dorsal and ventral pathway, the distinct frequency bands of these inputs can be leveraged to preserve the identity of the input source. In this way source-specific oscillatory activity in primate cortex can serve to establish and maintain “functionally labeled lines” for dynamically adjusting cortical information transfer and multiplexing converging sensory signals.

Dynamics of coherent activity between cortical areas defines a two-stage process of selective attention

“…Human psychophysical experiments also reinforce the point that gating functions of the dorsal stream prioritise spatial locations rather than specific features (27). The different frequencies for the two functions may also be functionally fortuitous, consistent with recent evidence that the brain may use different synchronising frequencies for different functions (20).…”

“…As can be seen in these three example cases and also when analysed across all those recording sessions where there was both significant LFP coherence and a multiunit response (MU) to the first grating, there was a significant latency difference between the spike response maxima and the coherence maxima in both areas (LIP: N=14 recording sites, p<0.001; MT: N=15, p< 0.001, Wilcoxon Signed Rank test). In MT, the peak spike response preceded the coherence maximum by 279 ms and in LIP by 341 ms. A recent study done in area MT also shows that synchrony seen at certain high gamma frequencies (180-220 Hz) represents sensory signals rather than a reflection of spike leakage (20), adding further credence to the importance of high gamma frequencies in information processing.…”

Phase of Firing Coding of Learning Variables across Prefrontal Cortex, Anterior Cingulate Cortex and Striatum during Feature Learning

“…These findings are consistent with a communication-through-coherence schema where upstream senders are more coherent with downstream readers when they successfully compete for representation (Bosman et al, 2012;Fries, 2015;. Yet it has remained unclear how such a scheme may operate when multiple items must be multiplexed and transmitted in the same recurrent network (Akam and Kullmann, 2014;Khamechian et al, 2019;Kopell et al, 2011;Palminteri et al, 2015;Siegel et al, 2009). Computationally, the multiplexing and the efficient transmission of information can operate in tandem when the temporal organization of activity is exploited at the sending and receiving site (Buzsáki, 2010;Hahn et al, 2019;Kumar et al, 2010;Luczak et al, 2015).…”

Attention strengthens across-trial pre-stimulus phase coherence in visual cortex, enhancing stimulus processing

“…increases with attention in a behaviorally relevant manner 16,27,30 . Moreover, recent investigations document a prominent role of low frequency oscillations, especially in the alpha/theta band, in attentional processing and shaping large-scale task-related functional networks of the brain [31][32][33] .…”

“…Attentional influences on neural responses in sensory cortex have been extensively documented; effects which reflect a multitude of aspects of cortical information processing 1-4 . Covertly directing attention towards the receptive field of a neuron in visual cortex enhances the neural responses even in the absence of visual stimulation 5,6 , alters the shape and profile of receptive fields 7-9 , modulates the variability and temporal structure of the neuron's firing patterns 10,11 , modulates inter-neuronal correlations to increase neural discriminability 12,13 and synchronizes neighboring neurons, presumably to better propagate information to downstream areas [14][15][16] .Attention has been suggested to exploit oscillatory neural activities, as well as oscillatory components of local field potentials (LFP), to enhance the efficacy of cortical processing 17-23 . LFPs represent synaptic activities of local cortical neuronal populations 24 .…”