| Abstract |
The present PhD thesis examines the neural mechanisms of selective visuοspatial attention and the role of the prefrontal cortex (PFC). Selective attention is central to cognition and adaptive behavior. In everyday life, we rely on instructions or knowledge of the location or features of the objects we search for in order to efficiently guide our attention. When location is the relevant instruction for the deployment of our attention, we refer to spatial attention, whereas when we use non-spatial features such as color, shape, size, of the relevant object, we refer to feature attention. Numerous studies have shown that attention has a profound influence on the representation of stimuli in the brain by selectively enhancing the representation of behaviorally relevant stimuli and suppressing the representation of distracting stimuli. The prefrontal cortex is considered to play a central role in this process with the frontal eye field (FEF) being a source of spatial attention signals that bias activity in visual areas in favor of attended stimuli. However, it is largely unknown whether prefrontal regions anterior to the FEF contribute to this process and through which mechanisms.
To examine the role of ventrolateral prefrontal cortex (vlPFC), a region anterior to the FEF, in spatial attention, we performed simultaneous extracellular recordings with multiple electrodes from vlPFC, FEF and visual area V4 in two macaques engaged in a covert spatial attention task. Monkeys were presented with an array of four gratings and were subsequently instructed by a central spatial cue to covertly attend to one of them and report its orientation using a joystick (post-cueing task). In another version of the same task, the spatial instruction was presented before the onset of the array and had to be memorized during a delay period (pre-cueing task). We recorded both spikes and local field potentials (LFPs).
In the post-cueing task, following the cue onset, spiking activity is modulated by spatial attention in all areas, but spatial attention effects emerge significantly earlier in PFC compared to V4. No significant difference in the onset of spatial attention effects is found between FEF and vlPFC. Within V4, LFP power and spike-LFP coherence, two measures of oscillatory activity and neural synchrony, are significantly enhanced by spatial attention in gamma frequencies (>30 Hz) whereas they are reduced in lower frequencies (4-30 Hz). Within PFC, theta power and coherence (4-8 Hz) are significantly enhanced with shifts of attention inside the receptive field (RF). Across the two areas, phase coupling between spikes and LFPs is only established when attention is directed to the common RF both in the theta and gamma frequency bands. Results from spike-LFP coherence between V4 and PFC and a Granger causality analysis between LFPs indicate a PFC origin for theta interactions and a V4 origin for gamma interactions. Notably, attentional effects in theta and gamma V4-PFC coherence show a significant positive correlation indicating a theta–gamma band interdependence. Effects in theta band coherence emerge significantly earlier compared to the effects in the gamma band coherence suggesting that theta interactions shape the subsequent gamma enhancement. Based on these results, we suggest that the early spike-theta locked input from PFC to V4 acts as a trigger in order to bias activity of the relevant population within V4.
In the absence of such an input to V4, during the condition that attention is directed outside the RF, local mechanisms within V4 seem to mediate the filtering of the distractor. Spikes and gamma oscillations within V4 are tightly locked to the phase of the theta oscillations as quantified by the increased spike-theta LFP coherence and theta–gamma phase-amplitude coupling. Stronger phase amplitude coupling during filtering of a distractor is associated with faster reaction times. Moreover, the theta phase of gamma enhancements differs between the two attention conditions in V4. Interestingly, a similar difference in the relative theta phase of LFPs across the two areas is seen between the two attention conditions. Importantly, the exact phase of theta-gamma coupling is behaviorally relevant as demonstrated by the analysis of error trials supporting the importance of the precise timing of these interactions for successful outcome. Thus, filtering of the unattended stimulus within V4 is likely mediated by three mechanisms: (a) by increased local competitive interactions expressed as an increase in theta LFP power, (b) by locally constraining spikes and gamma oscillations in time and (c) by limiting spikes and local gamma activity related to the distractor to a particular theta phase that may gate inputs to downstream areas and reduce processing downstream.
During the presentation of the cue, before the onset of the array and the subsequent delay period (pre-cueing task), spiking activity and theta power in PFC are robustly modulated by spatial attention. Specifically, theta power is increased for shifts of attention inside the RF transiently during 100-400 ms after the onset of the cue. Only within this time window, activities in PFC and V4 are functionally coupled in the theta frequency band and phase delays resemble the ones observed in the post-cueing task. This finding further supports the existence of an early time window where theta interactions are maximal between PFC and V4, are driven by PFC and are related to shifts of attention inside the common RF. Moreover, spatial attention effects in the firing activity of V4 emerge before the array onset in the absence of visual stimulation showing that the spatial instruction/attention position is encoded in V4 activity even in the absence of a visual stimulus inside the RF.
We suggest that this early theta interaction between PFC and V4 is crucial for biasing activity of the V4 population processing the stimulus inside the RF and overriding local mechanisms of competitive interactions within V4. Moreover, our results indicate that filtering of the distractor is largely implemented locally within V4 though lateral inhibition expressed as an increase in low frequency activity and particularly theta oscillatory activity.
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