Pop-out search instigates beta-gated feature selectivity enhancement across V4 layers

Visual search is a workhorse for investigating how attention interacts with processing of sensory information. Attentional selection has been linked to altered cortical sensory responses and feature preferences (i.e., tuning). However, attentional modulation of feature selectivity during search is largely unexplored. Here we map the spatiotemporal profile of feature selectivity during singleton search. Monkeys performed a search where a pop-out feature determined the target of attention. We recorded laminar neural responses from visual area V4. We first identified “feature columns” which showed preference for individual colors. In the unattended condition, feature columns were significantly more selective in superficial relative to middle and deep layers. Attending a stimulus increased selectivity in all layers but not equally. Feature selectivity increased most in the deep layers, leading to higher selectivity in extragranular layers as compared to the middle layer. This attention-induced enhancement was rhythmically gated in phase with the beta-band local field potential. Beta power dominated both extragranular laminar compartments, but current source density analysis pointed to an origin in superficial layers, specifically. While beta-band power was present regardless of attentional state, feature selectivity was only gated by beta in the attended condition. Neither the beta oscillation nor its gating of feature selectivity varied with microsaccade production. Importantly, beta modulation of neural activity predicted response times, suggesting a direct link between attentional gating and behavioral output. Together, these findings suggest beta-range synaptic activation in V4’s superficial layers rhythmically gates attentional enhancement of feature tuning in a way that affects the speed of attentional selection.

Columnar processing of border ownership in primate visual cortex

To understand a visual scene, the brain segregates figures from background by assigning borders to foreground objects. Neurons in primate visual cortex encode which object owns a border (border ownership), but the underlying circuitry is not understood. Here, we used multielectrode probes to record from border ownership-selective units in different layers in macaque visual area V4 to study the laminar organization and timing of border ownership selectivity. We find that border ownership selectivity occurs first in deep layer units, in contrast to spike latency for small stimuli in the classical receptive field. Units on the same penetration typically share the preferred side of border ownership, also across layers, similar to orientation preference. Units are often border ownership-selective for a range of border orientations, where the preferred sides of border ownership are systematically organized in visual space. Together our data reveal a columnar organization of border ownership in V4 where the earliest border ownership signals are not simply inherited from upstream areas, but computed by neurons in deep layers, and may thus be part of signals fed back to upstream cortical areas or the oculomotor system early after stimulus onset. The finding that preferred border ownership is clustered and can cover a wide range of spatially contiguous locations suggests that the asymmetric context integrated by these neurons is provided in a systematically clustered manner, possibly through corticocortical feedback and horizontal connections.

Brain state and cortical layer-specific mechanisms underlying perception at threshold

Identical stimuli can be perceived or go unnoticed across successive presentations, producing divergent behavioral readouts despite similarities in sensory input. We hypothesized that fluctuations in neurophysiological states in the sensory neocortex, which could alter cortical processing at the level of neural subpopulations, underlies this perceptual variability. We analyzed cortical layer-specific electrophysiological activity in visual area V4 during a cued attention task. We find that hit trials are characterized by a larger pupil diameter and lower incidence of microsaccades, indicative of a behavioral state with increased arousal and perceptual stability. Target stimuli presented at perceptual threshold evoke elevated multi-unit activity in V4 neurons in hit trials compared to miss trials, across all cortical layers. Putative excitatory and inhibitory neurons are strongly positively modulated in the input (IV) and deep (V & VI) layers of the cortex during hit trials. Excitatory neurons in the superficial cortical layers exhibit lower variability in hit trials. Deep layer neurons are less phase-locked to low frequency rhythms in hits. Hits are also characterized by greater interlaminar coherence between the superficial and deep layers in the pre-stimulus period, and a complementary pattern between the input layer and both the superficial and deep layers in the stimulus-evoked period. Taken together, these results indicate that a state of elevated levels of arousal and perceptual stability allow enhanced processing of sensory stimuli, which contributes to hits at perceptual threshold.

Methylphenidate as a causal test of translational and basic neural coding hypotheses

SUMMARYMost systems neuroscience studies fall into one of two categories: basic science work aimed at understanding the relationship between neurons and behavior, or translational work aimed at developing treatments for neuropsychiatric disorders. Here we use these two approaches to inform and enhance each other. Our study both tests hypotheses about basic science neural coding principles and elucidates the neuronal mechanisms underlying new, clinically relevant behavioral effects of systemically administered methylphenidate (Ritalin). We discovered that orally administered methylphenidate, used clinically to treat Attention Deficit Hyperactivity Disorder (ADHD) and generally to enhance cognition (Lakhan & Kirchgessner, 2012; Maher, 2008), increases spatially selective visual attention, enhancing visual performance at only the attended location. And as predicted by our previous work (Ni et al., 2018), we found that this causal manipulation enhances vision in rhesus macaques specifically when it decreases the mean correlated variability of neurons in visual area V4. Our findings demonstrate that the visual system is a platform for understanding the neural underpinnings of both complex cognitive processes (basic science) and neuropsychiatric disorders (translation). Addressing basic science hypotheses, our results are consistent with a scenario in which methylphenidate has cognitively specific effects by working through naturally selective cognitive mechanisms. Clinically, our findings suggest that the often staggeringly specific symptoms of neuropsychiatric disorders may be caused and treated by leveraging general mechanisms.

Laminar microcircuitry of visual cortex producing attention-associated electric fields

Cognitive operations are widely studied by measuring electric fields through EEG and ECoG. However, despite their widespread use, the component neural circuitry giving rise to these signals remains unknown. Specifically, the functional architecture of cortical columns which results in attention-associated electric fields has not been explored. Here we detail the laminar cortical circuitry underlying an attention-associated electric field often measured over posterior regions of the brain in humans and monkeys. First, we identified visual cortical area V4 as one plausible contributor to this attention-associated electric field through inverse modeling of cranial EEG in macaque monkeys performing a visual attention task. Next, we performed laminar neurophysiological recordings on the prelunate gyrus and identified the electric-field-producing dipoles as synaptic activity in distinct cortical layers of area V4. Specifically, activation in the extragranular layers of cortex resulted in the generation of the attention-associated dipole. Feature selectivity of a given cortical column determined the overall contribution to this electric field. Columns selective for the attended feature contributed more to the electric field than columns selective for a different feature. Lastly, the laminar profile of synaptic activity generated by V4 was sufficient to produce an attention-associated signal measurable outside of the column. These findings suggest that the top-down recipient cortical layers produce an attention-associated electric field capable of being measured extracranially and the relative contribution of each column depends upon the underlying functional architecture.

Columnar processing of border ownership in primate visual cortex

To understand a visual scene, the brain segregates figures from background by assigning borders to foreground objects. Neurons in primate visual cortex encode which object owns a border (border ownership), but the underlying circuitry is not understood. Here we used multielectrode probes to record from border ownership selective units in different layers in macaque visual area V4 to study the laminar organization and timing of border ownership selectivity. We find that border ownership selectivity occurs first in deep layer units, in contrast to spike latency for small stimuli in the classical receptive field. Units on the same penetration typically share the preferred side of border ownership, also across layers, similar to orientation preference. Units are often border ownership selective for a range of border orientations, where the preferred sides of border ownership are systematically organized in visual space. Together our data reveal a columnar organization of border ownership in V4 where the earliest border ownership signals are not simply inherited from upstream areas, but computed by neurons in deep layers, and may thus be part of signals fed back to upstream cortical areas or the oculomotor system early after stimulus onset. The finding that preferred border ownership is clustered and can cover a wide range of spatially contiguous locations, suggests that the asymmetric context integrated by these neurons is provided in a systematically clustered manner, possibly through corticocortical feedback and horizontal connections.

Neuronal correlates of attentional selectivity and intensity in visual area V4 are invariant of motivational context

Flexibly switching attentional strategies is crucial for adaptive behavior in changing environments. Depending on the context, task demand employs different degrees of the two fundamental components of attention- attentional selectivity (preferentially attending to one location in visual space) and effort (the total non-selective intensity of attention). Neuronal responses in the visual cortex that show modulation with changes in either selective attention or effort are reported to partially represent motivational aspect of the task context. The relative contributions and interactions of these two components of attention to modulate neuronal signals and their sensitivity to distinct motivational drives are poorly understood. To address this question, we independently controlled monkeys' spatially selective attention and non-selective attentional intensity in the same experimental session during a novel visual orientation change detection task. Attention was controlled either by adjusting the relative difficulty of the orientation changes at the two locations or by the reward associated with stimuli at two locations while simultaneously recording spikes from populations of neurons in area V4. We found that V4 neurons are robustly modulated by either selective attention or attentional intensity. Notably, as attentional selectivity for a neuron's receptive field location decreased, its responses became weaker, despite an increase in the animal's overall attentional intensity. This strong interaction between attentional selectivity and intensity could be identified in single trial spike trains. A simple divisive normalization of spatially distributed attention performances can explain the interaction between attention components well at the single neuron level. The effects of attentional selectivity and attentional intensity on neuronal responses were the same regardless of whether the changes were motivated by reward or task difficulty. These results provide a detailed cellular-level mechanism of how fundamental components of attention integrate and affect sensory processing in varying motivational and stimulus contexts.

Color Modulates Feature Integration

Bayesian models of object recognition propose the resolution of ambiguity through probabilistic integration of prior experience with available sensory information. Color, even when task-irrelevant, has been shown to modulate high-level cognitive control tasks. However, it remains unclear how color modulations affect lower-level perceptual processing. We investigated whether color affects feature integration using the flash-jump illusion. This illusion occurs when an apparent motion stimulus, a rectangular bar appearing at different locations along a motion trajectory, changes color at a single position. Observers misperceive this color change as occurring farther along the trajectory of motion. This mislocalization error is proposed to be produced by a Bayesian perceptual framework dependent on responses in area V4. Our results demonstrated that the color of the flash modulated the magnitude of the flash-jump illusion such that participants reported less of a shift, i.e., a more veridical flash location, for both red and blue flashes, as compared to green and yellow. Our findings extend color-dependent modulation effects found in higher-order executive functions into lower-level Bayesian perceptual processes. Our results also support the theory that feature integration is a Bayesian process. In this framework, color modulations play an inherent and automatic role as different colors have different weights in Bayesian perceptual processing.