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.

How neural activity is linked to behavior is a critical question in neural engineering and cognitive neurosciences. It is crucial to predict behavior as early as possible, to plan a machine response in real-time brain computer interactions. However, previous studies have studied the neural readout of behavior only within a short time before the action is performed. This leaves unclear, if the neural activity long before a decision could predict the upcoming behavior. By recording extracellular neural activities from the visual cortex of behaving rhesus monkeys, we show that: (1) both, local field potentials (LFPs) and the rate of neural spikes long before (>2 s) a monkey responds to a change, foretell its behavioral performance in a spatially selective manner; (2) LFPs, the more accessible component of extracellular activity, are a stronger predictor of behavior; and (3) LFP amplitude is positively correlated while spiking activity is negatively correlated with behavioral reaction time (RT). These results suggest that field potentials could be used to predict behavior way before it is performed, an observation that could potentially be useful for brain computer interface applications, and that they contribute to the sensory neural circuit’s speed in information processing.

The idea that a flexible behavior relies on synchronous neural activity within intra-and inter-associated cortical areas has been a matter of intense research in human and animal neuroscience. The neurophysiological mechanisms underlying this behavioral correlate of the synchronous activity are still unknown. It has been suggested that the strength of neural synchrony at the level of population is an important neural code to guide an efficient transformation of the sensory input into the behavioral action. In this study, we have examined the non-linear synchronization between neural ensembles in area MT of the macaque visual cortex by employing a non-linear cross-frequency coupling technique, namely bicoherence. We trained a macaque monkey to detect a brief change in the cued stimulus during a visuomotor detection task. The results show that the non-linear phase synchronization in the high-gamma frequency band (100-250 Hz) predicts the animal's reaction time. The strength of non-linear phase synchronization is selective to the target stimulus location. In addition, the non-linearity characteristics of neural synchronization are selectively modulated when the monkey covertly attends to the stimulus inside the neuron's receptive field. This additional evidence indicates that non-linear neuronal synchronization may be affected by a cognitive function like spatial attention. Our neural and behavioral observations reflect that two crucial processes may be involved in processing of visuomotor information in area MT: (I) a non-linear cortical process (measured by the bicoherence) and (II) a linear process (measured by the spectral power).

Research in cognitive neuroscience has renewed the idea that brain oscillations are a core organization implicated in fundamental brain functions. Growing evidence reveals that the characteristic features of these oscillations, including power, phase and frequency, are highly non-stationary, fluctuating alongside alternations in sensation, cognition and behavior. However, there is little consensus on the functional implications of the instantaneous frequency variation in cortical excitability and concomitant behavior. Here, we capitalized on intracortical electrophysiology in the macaque monkey’s visual area MT performing a visuospatial discrimination task with visual cues. We observed that the instantaneous frequency of the theta–alpha oscillations (4–13 Hz) is modulated among specific neurons whose RFs overlap with the cued stimulus location. Interestingly, we found that such frequency modulation is causally correlated with MT excitability at both scales of individual and ensemble of neurons. Moreover, studying the functional relevance of frequency variations indicated that the average theta–alpha frequencies foreshadow the monkey’s reaction time. Our results also revealed that the neural synchronization strength alters with the average frequency shift in theta–alpha oscillations, suggesting frequency modulation is critical for mutually adjusting MTs’ rhythms. Overall, our findings propose that theta–alpha frequency variations modulate MT’s excitability, regulate mutual neurons’ rhythmicity and indicate variability in behavior.