Strength of Response Suppression to Distracter Stimuli Determines Attentional-Filtering Performance in Primate Prefrontal Neurons

SummaryNeurons in the primate dorsolateral prefrontal cortex (dlPFC) filter attended targets distinctly from distracters through their response rates. The extent to which this ability correlates with the organism's performance, and the neural processes underlying it, remain unclear. We trained monkeys to attend to a visual target that differed in rank along a color-ordinal scale from that of a distracter. The animals' performance at focusing attention on the target and filtering out the distracter improved as ordinal distance between the stimuli increased. Importantly, dlPFC neurons also improved their filtering performance with increasing ordinal target-distracter distance; they built up their response rate in anticipation of the target-distracter onset, and then units encoding target representations increased their firing rate by similar amounts, whereas units encoding distracter representations gradually suppressed their rates as the interstimulus ordinal distance increased. These results suggest that attentional-filtering performance in primates relies upon dlPFC neurons' ability to suppress distracter representations

Prefrontal neurons of opposite spatial preference display distinct target selection dynamics.

Neurons in the primate dorsolateral prefrontal cortex (dlPFC) of one hemisphere are selective for the location of attended targets in both visual hemifields. Whether dlPFC neurons with selectivity for opposite hemifields directly compete with each other for target selection or instead play distinct roles during the allocation of attention remains unclear. We explored this issue by recording neuronal responses in the right dlPFC of two macaques while they allocated attention to a target in one hemifield and ignored a distracter on the opposite side. Forty-nine percent of the recorded neurons were target location selective. Neurons selective for contralateral targets (58%) systematically discriminated targets from distracters faster than neurons selective for ipsilateral targets (42%). Additionally, during trials in which sensory stimulation remained the same but both stimuli were task irrelevant and animals were required to detect a change in the color of a fixation spot, contralateral neurons still reliably discriminated the putative target from the distracter, whereas ipsilateral neurons did not. The latter result indicates that target-distracter discrimination by contralateral neurons could occur independently of discrimination by ipsilateral cells; thus, the two cell types may represent two different components of the prefrontal circuitry underlying the allocation of attention to targets in the presence of distracters. Moreover, the response of both contralateral and ipsilateral neurons to a single target was substantially reduced by the presence of a distracter in the contralateral hemifield. This result suggests that the presence of the distracter triggered inhibitory interactions within the dlPFC circuitry that suppressed responses to the attended target

Sharp emergence of feature-selective sustained activity along the dorsal visual pathway.

Sustained activity encoding visual working memory representations has been observed in several cortical areas of primates. Where along the visual pathways this activity emerges remains unknown. Here we show in macaques that sustained spiking activity encoding memorized visual motion directions is absent in direction-selective neurons in early visual area middle temporal (MT). However, it is robustly present immediately downstream, in multimodal association area medial superior temporal (MST), as well as and in the lateral prefrontal cortex (LPFC). This sharp emergence of sustained activity along the dorsal visual pathway suggests a functional boundary between early visual areas, which encode sensory inputs, and downstream association areas, which additionally encode mnemonic representations. Moreover, local field potential oscillations in MT encoded the memorized directions and, in the low frequencies, were phase-coherent with LPFC spikes. This suggests that LPFC sustained activity modulates synaptic activity in MT, a putative top-down mechanism by which memory signals influence stimulus processing in early visual cortex

Attentional filtering of visual information by neuronal ensembles in the primate lateral prefrontal cortex.

The activity of neurons in the primate lateral prefrontal cortex (LPFC) is strongly modulated by visual attention. Such a modulation has mostly been documented by averaging the activity of independently recorded neurons over repeated experimental trials. However, in realistic settings, ensembles of simultaneously active LPFC neurons must generate attentional signals on a single-trial basis, despite the individual and correlated variability of neuronal responses. Whether, under these circumstances, the LPFC can reliably generate attentional signals is unclear. Here, we show that the simultaneous activity of neuronal ensembles in the primate LPFC can be reliably decoded to predict the allocation of attention on a single-trial basis. Decoding was sensitive to the noise correlation structure of the ensembles. Additionally, it was resilient to distractors, predictive of behavior, and stable over weeks. Thus, LPFC neuronal ensemble activity can reliably encode attention within behavioral time frames, despite the noisy and correlated nature of neuronal activity

Developing optogenetics/electrophysiology applications for studying cognitive impairment during stress

We will develop cutting-edge techniques to: precisely measure and artificially manipulate the activity of CRH neurons in the PFC, and measure small and local releases of CRH by these neurons. The success of our project will open the door to understand the neural mechanisms for how stress impairs cognitive functions and how it may contribute to mental disorders.https://ir.lib.uwo.ca/brainscanprojectsummaries/1035/thumbnail.jp

The role of the basolateral amygdala in gaze avoidance behaviour

We are researching the neural circuits involved in human social interactions and how they are affected during mental disease, in particular the circuits involved in the pattern of eye movements (known as gaze behaviour) in social settings.https://ir.lib.uwo.ca/brainscanprojectsummaries/1016/thumbnail.jp

Development of Virtual Gaming Environments for Functional Magnetic Resonance Imaging

The goal of this project is to develop, validate and test three aspects of a 3D video game environment for neuroscience.https://ir.lib.uwo.ca/brainscanprojectsummaries/1031/thumbnail.jp

Multi-area organization of saccade-evoked traveling waves

In this project, we will employ new, large-scale electrophysiological recording techniques to sample widely across the visual system. It will allow us to test our hypothesis that neural traveling waves coordinated across multiple areas contribute to perceptual stability during eye movements. Using our newly developed signal processing technique to track traveling waves moment-by-moment in noisy multichannel data, we will detect and quantify them across multiple visual areas.https://ir.lib.uwo.ca/brainscanprojectsummaries/1040/thumbnail.jp

The effects of methylphenidate (Ritalin) on the neurophysiology of the monkey caudal prefrontal cortex

© 2019 Tremblay et al. Methylphenidate (MPH), commonly known as Ritalin, is the most widely prescribed drug worldwide to treat patients with attention deficit disorders. Although MPH is thought to modulate catecholamine neurotransmission in the brain, it remains unclear how these neurochemical effects influence neuronal activity and lead to attentional enhancements. Studies in rodents overwhelmingly point to the lateral prefrontal cortex (LPFC) as a main site of action of MPH. To understand the mechanism of action of MPH in a primate brain, we recorded the responses of neuronal populations using chronic multielectrode arrays implanted in the caudal LPFC of two macaque monkeys while the animals performed an attention task (N 2811 neuronal recordings). Over different recording sessions (N 55), we orally administered either various doses of MPH or a placebo to the animals. Behavioral analyses revealed positive effects of MPH on task performance at specific doses. However, analyses of individual neurons activity, noise correlations, and neuronal ensemble activity using machine learning algorithms revealed no effects of MPH. Our results suggest that the positive behavioral effects of MPH observed in primates (including humans) may not be mediated by changes in the activity of caudal LPFC neurons. MPH may enhance cognitive performance by modulating neuronal activity in other regions of the attentional network in the primate brain