Neural correlates of perceptual transitions during binocular flash suppression

Abstract

Neural correlates of visual awareness have been attracting scientists’ interest for decades. A central question for many students has been at which stage of brain processing the resolution of perceptual ambiguities occurs. Discovering which aspects of neural activity underlie our subjective percepts and not simply the sensory input has also fascinated many researchers for a long time. Bistable and multistable perception phenomena demonstrated great experimental potential to address this question in primary visual cortex (V1) and multiple higher cortical areas including temporal and prefrontal cortices in humans and macaques. However, the role of single neurons in parietal cortical areas in perceptual transitions has not been explored in macaques by the time of this work. Also, the role that area V1 plays in perception has been a subject of debate, as the magnitude of perceptual modulations differed substantially in single-cell and imaging studies. In this thesis, we took a step further and explored the role of parietal visual areas in perceptual transitions during binocular flash suppression (BFS). We also searched for another coding scheme in V1 in addition to firing rate modulation, which may be responsible for larger modulations observed in human studies. Furthermore, we compared the extent to which neurons in V1 modulate by perception under anesthetized conditions and compared with awake passively fixating animals during the BFS paradigm in order to highlight the possible role of task in this controversy. For the first set of experiments, we recorded extracellular activity from visual units in lateral intraparietal area (LIP) of the macaque brain under the conditions of BFS. We found that LIP neurons exhibit two type of responses to the perceptual changes, possibly responsible for two distinct underlying processes: a fast transient component that is a good candidate of feedback carrying higher order visual information to the early cortical circuits, and a tonic response, which is moderately modulated by perception and becomes selective to the visual stimuli by manipulating reward size. Next, we analyzed a large dataset of single- and multi-unit activity in V1 concurrently recorded with the local field potentials (LFP) during BFS stimulation. We found that spike-field coherence (SFC) in V1 was correlated with subjective perception. Of particular interest, this correlation was also found in the absence of significant modulations in firing rate. We conjectured that SFC plays a leading role in initiating the competition in V1. Finally, we analyzed comparable spiking data collected during anesthesia and awake passive fixation conditions from four macaque monkeys and showed that the modulation of firing rates in V1 upon perceptual suppression during BFS is comparable in both conditions. We concluded that active engagement in a task is critical to boost firing rate modulations in V1 to the level reported in human studies. Taken together, our work confirms that a distributed network of cortical regions is responsible for the resolution of perceptual rivalry during bistable conditions. This includes areas as early as primary visual cortex and higher processing stages like fronto-parietal areas. However, the strength of these modulations may depend on the level of engagement of subjects in an active task. We demonstrated that modulation of neural activity in the firing rates during passive fixation is essentially comparable to the anesthetized condition in V1. In addition, we provided evidence that modulation of firing rate is not the only neural correlate of perception and showed that neural synchronization in V1 can reflect perceptual state even in the absence of firing rate modulations. Orchestration of coherent activity observed in V1 can be triggered by the fast feedback signals from higher visual areas like LIP. Our work, preempts fascinating studies in the future to explore the network characteristics of LIP itself, and the relationship between task engagement and SFC variations in early and higher visual areas.

Mittels bildgebender Verfahren wurde die Beteiligung eines weit verteilten Netzwerkes von Hirnregionen, inklusive dem primären visuellen Kortex (V1) und dem frontoparietalen kortikalen Netzwerk, beim Wechsel in der Wahrnehmung im Zusammenhang mit bistabilen und multistabilen Phänomenen nachgewiesen. Auf dem Niveau von einzelnen Neuronen wurde die Rolle des parietalen Kortexes beim Wahrnehmungswechsel allerdings noch nicht sehr gut erforscht. Darüber hinaus ist die Rolle der Region um V1 in der Wahrnehmungsorganisation immer noch viel diskutiert. In dieser Arbeit haben wir den Beitrag des parietalen Kortex im Wahrnehmungswechsel während der so genannten „binokular flash suppression“ (BFS) untersucht. Weiterhin haben wir die Hypothese, dass synchronisierte Aktivität in V1 Information über die Wahrnehmung überträgt, getestet. Darüber hinaus haben wir das Ausmaß der wahrnehmungsabhängigen Modulierung von Neuronen in V1 zwischen anästhesierten und wachen, passiv fixierenden Tieren verglichen. Unsere Arbeit bestätigt, dass ein weit verteiltes Netzwerk von kortikalen Regionen zur Auflösung der Rivalität zwischen den Wahrnehmungen bistabiler Zustände beiträgt. Das beinhaltet sowohl niedere Regionen wie V1 als auch höhere Verarbeitungsstufen wie die laterale intraparietale Region (LIP). Allerdings könnte das Ausmaß der Modulierung der Neurone stark davon abhängen, wie engagiert sich das Tier in der aktiven Aufgabe verhält. Wir konnten darlegen, dass die Modulierung der neuronalen Feuerrate in V1 während der passiven Fixierung und unter Anästhesie generell vergleichbar ist. Schließlich konnten wir Belege dafür liefern, dass die Modulierung der Feuerrate nicht das einzige neuronale Korrelat der Wahrnehmung ist und dass neuronale Synchonisierung in V1 ein Stadium der Wahrnehmung wiederspiegeln kann obwohl keine signifikante Modulierung der Feuerrate statt findet. Das Dirigieren kohärenter Aktivität, wie sie in V1 beobachtet wurde, kann durch schnelle Rückinformation von höheren visuellen Arealen wie LIP initiiert werden.