The role of association cortical networks in visual consciousness

Introduction and Scientific Aims

The neural signature of visual consciousness has been detected in the electrical activity of multiple cortical areas across the visual hierarchy, during tasks that permit a dissociation of purely sensory stimulation from subjective perception. In the past, single unit and local field potential (LFP) recordings were mainly employed to define the contribution of different cortical areas in visual awareness. However, understanding the dynamics of cortical networks during subjective visual perception at a local microcircuit level but also in a global scale could reveal unknown aspects of neural activity that are more directly related to the emergence of visual awareness. Which are then these features of neuronal activity that – if examined at a global scale – may potentially uncover the mechanisms responsible for the subjective experiences that define consciousness? We address these questions using a combination of behavioral, electrophysiological and computational methods.

Converging evidence from psychophysical, functional imaging and electrophysiological studies points to a crucial role of non-sensory, association cortical areas in subjective visual perception. These areas are thought to modulate neuronal activity in primary, sensory and lower associational areas through feedback connections and inter-level interactions in general. The main goal of this project is first to describe the local population dynamics of neural activity in the prefrontal and temporal cortices as well as the corticocortical interactions between these two areas that relate to the behavior of animals reporting what they perceive at any given time. In this first step a detailed understanding of cortical phenomena like intrinsic noise and spatiotemporally organized electrical activity is important, as it can reveal some of the emerging neural properties underlying visual awareness. The findings of these investigations will be the seed for future research of larger networks examined with a combination of imaging and multi-site electrophysiology techniques.

Methods

We use extracellular multielectrode and tetrode electrophysiological recordings coupled with behavioral tasks that introduce ambiguous visual stimulation in macaque monkeys. Monkeys are trained to report their subjective stimulus experience by pulling levers during tasks like binocular rivalry and binocular flash suppression. These paradigms allow a dissociation of sensory stimulation from subjective perception, thus permitting a similar dissociation of the simultaneously recorded neuronal activity. We use single unit and LFP recordings in single sites to probe the contribution of cortical areas to conscious perception. Our neurophysiological data are then used to constrain theoretical models on dynamic complex systems studying the factors that mediate spontaneous perceptual switches. Furthermore, in our effort to better understand the spatiotemporal patterns of spontaneous activity in the areas of interest and how these patterns are modulated during conscious visual perception, we study neural activity with large electrode-arrays that provide high spatial resolution.

Optimization of this methodology is currently done by recording in the prefrontal cortex during anesthesia. Novel analytical tools are also developed to cluster the recorded spatiotemporal patterns of neural activity. Finally, we develop new electrophysiological recording methods that allow excellent single unit isolation and therefore the monitoring of large neuronal populations in areas of the temporal cortex.

A. Single unit tetrode recordings in the lateral prefrontal cortex.

B. Modulation of neuronal discharges during sensory stimulation and ambiguous visual perception.

C. Utah-multielectrode array recordings in the inferior convexity of the lateral prefrontal cortex.

Students

Vishal Kapoor (Binocular Rivalry, PFC-IT interactions and development of tetrode technology)

Britni Crocker (information theoretic analysis of neural signals in the macaque PFC and functional imaging of the PFC)

Collaborators

Theoretical modeling of bistable perception

Prof. Dr. Gustavo Deco

(Computational Neuroscience Group, Universitat Pompeu Fabra, Barcelona, Spain)

Panagiota Theodoni

(Computational Neuroscience Group, Universitat Pompeu Fabra, Barcelona, Spain)

Spatiotemporal mapping of neuronal activity in the macaque PFC

Dr. Michel Besserve

(MPI for Biological Cybernetics, Tubingen, Germany)

Dr. Stefano Panzeri

(Italian Institute of Technology, Robotics, Brain and Cognitive Sciences Department, Genova, Italy)

Dr. Andreas Tolias

(Baylor College of Medicine, Department of Neuroscience, Houston, U.S.A)

Functional Imaging of the macaque PFC

Dr. Jozien Goense

(MPI for Biological Cybernetics, Tubingen, Germany)

Publications

Peer-reviewed articles

Theodoni, P., Panagiotaropoulos, T.I., Kapoor, V., Logothetis, N.K., and Deco, G. (2011). Cortical microcircuit dynamics mediating binocular rivalry: The role of adaptation in inhibition. Front Hum Neurosci 5, 145.

Schmid, M.C., Panagiotaropoulos, T., Augath, M.A., Logothetis, N.K., and Smirnakis, S.M. (2009). Visually driven activation in macaque areas V2 and V3 without input from the primary visual cortex. PLoS One 4, e5527.

Panagiotaropoulos, T.I., Deco G., Kapoor, V. Logothetis, N.K.(2012).Neuronal discharges and gamma oscillations explicitly reflect conscious visual perception in the lateral prefrontal cortex. Neuron (in press)

Deco G., Panagiotaropoulos T.I., Kapoor, V., Logothetis, N.K. (submitted). Neuronal correlates of binocular flash suppression and the dynamical range of perceptual rivalry.

Book Chapters

Panagiotaropoulos, T.I. and Logothetis N.K. (in press). Multistable visual perception as a gateway to the neural correlates of phenomenal consciousness. The scope and limits of neuroscientific analysis. in The Handbook of Experimental Phenomenology (Ed. L. Albertazzi).

Panagiotaropoulos, T.I., Logothetis N.K. and Keliris, G.A. (in press) Neural approaches to perceptual organization. in The Handbook of Computational Perceptual Organization (Eds. Gepshtein-Maloney).

Special Research Topic in the Frontiers in Human Neuroscience

Binocular Rivarly: A Gateway to Consiousness

(co-hosted with G.A. Keliris, A. Maier and N. Tsuchiya)

For a full publication list including previous work in early experiences, stress, learning and memory click here

The role of lateral prefrontal cortex in conscious visual perception

Our results show that neuronal activity in the lateral prefrontal cortex strongly correlates with subjective visual perception. The responses of small neuronal populations are as selective and perception-driven as those reported in the temporal cortex; yet we find that their dynamic profile could be distinctly different from that of IT neurons, suggesting that these two regions may have differential contribution in visual awareness.

Cortical microcircuit dynamics mediating binocular rivalry

Psychophysical and electrophysiological data are used to constrain dynamic models of bistable perception. The predictions provided by the combination of theoretical and experimental results formulate new experimental questions.

Examination of functional interactions between prefrontal and inferotemporal cortex during binocular rivalry

Two monkeys are currently trained to report spontaneous binocular rivalry. The functional interactions between PFC and IT cortex are currently probed during externally induced perceptual switches using binocular flash suppression

Spatiotemporal mapping of rhythmic activity in the macaque lateral prefrontal cortex

Large-scale spatiotemporal patterns of spontaneous and visually driven neuronal activity in the lateral prefrontal cortex are characterized.

Information theoretic analysis of electrophysiological signals in the macaque prefrontal cortex.

We quantify the information conveyed by LFP's and neuronal discharges in the lateral prefrontal cortex during visual stimulation.

Subcortical control of cortical network dynamics

Stimulation of thalamic nuclei will be used to control the dynamics of electrical activity in the cortex.