Ripples in macaque V1 and V4 are modulated by top-down visual attention.

Sharp-wave ripples (SWRs) are highly synchronous neuronal activity events. They have been predominantly observed in the hippocampus during offline states such as pause in exploration, slow-wave sleep, and quiescent wakefulness. SWRs have been linked to memory consolidation, spatial navigation, and spatial decision-making. Recently, SWRs have been reported during visual search, a form of remote spatial exploration, in macaque hippocampus. However, the association between SWRs and multiple forms of awake conscious and goal-directed behavior is unknown. We report that ripple activity occurs in macaque visual areas V1 and V4 during focused spatial attention. The occurrence of ripples is modulated by stimulus characteristics, increased by attention toward the receptive field, and by the size of the attentional focus. During attention cued to the receptive field, the monkey's reaction time in detecting behaviorally relevant events was reduced by ripples. These results show that ripple activity is not limited to hippocampal activity during offline states, rather they occur in the neocortex during active attentive states and vigilance behaviors.

Cell class-specific modulation of attentional signals by acetylcholine in macaque frontal eye field.

Attention is critical to high-level cognition, and attentional deficits are a hallmark of cognitive dysfunction. A key transmitter for attentional control is acetylcholine, but its cellular actions in attention-controlling areas remain poorly understood. Here we delineate how muscarinic and nicotinic receptors affect basic neuronal excitability and attentional control signals in different cell types in macaque frontal eye field. We found that broad spiking and narrow spiking cells both require muscarinic and nicotinic receptors for normal excitability, thereby affecting ongoing or stimulus-driven activity. Attentional control signals depended on muscarinic, not nicotinic receptors in broad spiking cells, while they depended on both muscarinic and nicotinic receptors in narrow spiking cells. Cluster analysis revealed that muscarinic and nicotinic effects on attentional control signals were highly selective even for different subclasses of narrow spiking cells and of broad spiking cells. These results demonstrate that cholinergic receptors are critical to establish attentional control signals in the frontal eye field in a cell type-specific manner.

Distinct feedforward and feedback pathways for cell-type specific attention effects.

Selective attention is thought to depend on enhanced firing activity in extrastriate areas. Theories suggest that this enhancement depends on selective inter-areal communication via gamma (30-80 Hz) phase-locking. To test this, we simultaneously recorded from different cell types and cortical layers of macaque V1 and V4. We find that while V1-V4 gamma phase-locking between local field potentials increases with attention, the V1 gamma rhythm does not engage V4 excitatory-neurons, but only fast-spiking interneurons in L4 of V4. By contrast, attention enhances V4 spike-rates in both excitatory and inhibitory cells, most strongly in L2/3. The rate increase in L2/3 of V4 precedes V1 in time. These findings suggest enhanced signal transmission with attention does not depend on inter-areal gamma phase-locking and show that the endogenous gamma rhythm has cell-type- and layer-specific effects on downstream target areas. Similar findings were made in the mouse visual system, based on opto-tagging of identified interneurons.

Stimulus dependence of directed information exchange between cortical layers in macaque V1.

Perception and cognition require the integration of feedforward sensory information with feedback signals. Using different sized stimuli, we isolate spectral signatures of feedforward and feedback signals, and their effect on communication between layers in primary visual cortex of male macaque monkeys. Small stimuli elicited gamma frequency oscillations predominantly in the superficial layers. These Granger-causally originated in upper layer 4 and lower supragranular layers. Unexpectedly, large stimuli generated strong narrow band gamma oscillatory activity across cortical layers. They Granger-causally arose in layer 5, were conveyed through layer six to superficial layers, and violated existing models of feedback spectral signatures. Equally surprising, with large stimuli, alpha band oscillatory activity arose predominantly in granular and supragranular layers and communicated in a feedforward direction. Thus, oscillations in specific frequency bands are dynamically modulated to serve feedback and feedforward communication and are not restricted to specific cortical layers in V1.

An Open Resource for Non-human Primate Optogenetics.

Optogenetics has revolutionized neuroscience in small laboratory animals, but its effect on animal models more closely related to humans, such as non-human primates (NHPs), has been mixed. To make evidence-based decisions in primate optogenetics, the scientific community would benefit from a centralized database listing all attempts, successful and unsuccessful, of using optogenetics in the primate brain. We contacted members of the community to ask for their contributions to an open science initiative. As of this writing, 45 laboratories around the world contributed more than 1,000 injection experiments, including precise details regarding their methods and outcomes. Of those entries, more than half had not been published. The resource is free for everyone to consult and contribute to on the Open Science Framework website. Here we review some of the insights from this initial release of the database and discuss methodological considerations to improve the success of optogenetic experiments in NHPs.

Influence of visually guided tracking arm movements on single cell activity in area MT.

The behavioral relevance of neuronal activity in primate area MT for motion perception and control of visually guided eye movements is well documented. The projections of area MT comprise connections to subcortical structures and to the parietal network, both of which play a role in visuospatial transformation for guiding eyes and hands. Here, we have investigated, whether area MT is involved in the network needed to control visually guided arm movements. Our results show that half of the neurons tested significantly modulated their activity during visually guided arm movements. We conclude that the main reason for the neuronal modulation is not the arm movement per se, but the use of information from MT for visual feedback in the tracking movement. Moreover, control experiments show that attentional effects cannot solely cause the neuronal modulation. Thus, our study provides strong evidence that area MT is involved in processing visual information for visually guided manual tracking movements.