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.
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.
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.
Relevant Publications/Conference Abstracts
Panagiotaropoulos TI, Theodoni P, Kapoor V, Deco G, Logothetis NK. (2014). Decorrelated discharge fluctuations in prefrontal microcircuits during visual consciousness. (in preparation).
Panagiotaropoulos TI, Logothetis NK and Keliris GA. (2014) Neural approaches to perceptual organization. in The Handbook of Computational Perceptual Organization, Eds. Gepshtein-Maloney. (in press)
see co-organized/co-chaired with K. Takahashi, T.Zanos, M. Besserve.
see (co-hosted with G.A. Keliris, A. Maier and N. Tsuchiya)
(Binocular Rivalry, PFC-IT interactions and development of tetrode technology)
(Neural mechanisms of predictive coding)
(information theoretic analysis of neural signals in the macaque PFC and functional imaging of the PFC)
Theoretical modeling of bistable perception
Computational Neuroscience Group, Universitat Pompeu Fabra, Barcelona, Spain
Spatiotemporal mapping of neuronal activity in the macaque PFC
MPI for Biological Cybernetics, Tubingen, Germany
University of Glasgow, Scotland
Baylor College of Medicine, Department of Neuroscience, Houston, U.S.A
Functional Imaging of the macaque PFC
MPI for Biological Cybernetics, Tubingen, Germany
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; therefore the content of conscious visual perception is reliably represented in the neuronal activity of at least two association cortical areAs.
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.
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
Large-scale spatiotemporal patterns of spontaneous and visually driven neuronal activity in the lateral prefrontal cortex are characterized.
We quantify the information conveyed by LFP's and neuronal discharges in the lateral prefrontal cortex during visual stimulation.
MPI for Biological Cybernetics
Spemanstrasse 38, 72076, Tubingen, Germany
2006-2012 Postdoctoral fellow Max Planck Institute for Biological Cybernetics
2005 Phd in Cognitive Science National & Kapodistrian University of Athens.
2002 MSc in Cognitive Science National & Kapodistrian University of Athens.
1999 BA in Psychology Panteion University of Athens.
1997-98 Training in Adolescent Psychopathology Department of Adolescent Psychiatry, General Hospital of Athens G.Gennimatas
Peer-reviewed articles (in chronological order)
- Safavi S, Kapoor V, Logothetis NK, Panagiotaropoulos TI. (2014) Is the frontal lobe involved in conscious perception? Front Psychol 5:1063
- Panagiotaropoulos TI, Kapoor V, Logothetis NK. (2014) Subjective visual perception: From local processing to emergent phenomena of brain activity . Philos Trans R Soc Lond B Biol Sci 369(1641) 1-13.
- Panagiotaropoulos TI, Kapoor V, Logothetis NK, Deco G. (2013). A Common Neurodynamical Mechanism Could Mediate Externally Induced and Intrinsically Generated Transitions in Visual Awareness. PLoS One 8(1), e53833.
- Panagiotaropoulos TI, Kapoor V, Logothetis NK. (2013). Desynchronization and rebound of beta oscillations during conscious and unconscious local neuronal processing in the macaque lateral prefrontal cortex. Front Psychol 4:603.
- Kapoor V, Krampe E, Klug A, Logothetis NK, Panagiotaropoulos TI. (2013). Development of a Multi-Tetrode Drive for deep structure - high quality electrophysiological recordings in the macaque brain. J Neurosci Methods 216(1):43-8.
- Stamatakis A, Diamantopoulou A, Panagiotaropoulos TI, Raftogianni A, Stylianopoulou F. (2013) Effects of an early experience involving training in a T-maze under either denial or receipt of expected reward through maternal contact. Front Endocrinol 4, 178.
- Maier A, Panagiotaropoulos TI, Tsuchiya N, Keliris GA. (2012). Introduction to research topic - binocular rivalry: a gateway to studying consciousness. Front Hum Neurosci 6, 263.
- Panagiotaropoulos TI, Deco G, Kapoor V, Logothetis NK. (2012). Neuronal Discharges and Gamma Oscillations Explicitly Reflect Visual Consciousness in the Lateral Prefrontal Cortex. Neuron 74, 924-935.
- Theodoni P, Panagiotaropoulos TI, Kapoor V, Logothetis NK, Deco G. (2011). Cortical microcircuit dynamics mediating binocular rivalry: the role of adaptation in inhibition. Front Hum Neurosci 5, 145.
- Diamantopoulou A, Stamatakis A, Panagiotaropoulos T, Stylianopoulou F. (2011). Reward or its denial during the neonatal period affects adult spatial memory and hippocampal phosphorylated cAMP response element-binding protein levels of both the neonatal and adult rat. Neuroscience 181, 89-99.
- Schmidt MC, Panagiotaropoulos T, Augath M, Logothetis NK, Smirnakis SM. (2009). Retinotopic activation of macaque area V2 without input from primary visual cortex. PLoS One 4(5), e5527.
- Panagiotaropoulos T, Diamantopoulou A, Stamatakis A, Dimitropoulou M, Stylianopoulou F. (2009). Learning of a T-maze by rat pups when contact with the mother is either permitted or denied. Neurobiol Learn Mem 91, 2-12.
- Savvaki M*, Panagiotaropoulos T*, Stamatakis A, Sargiannidou I, Karatzioula P, Watanabe K, Stylianopoulou F, Karagogeos D, Kleopa KA. (2008). Impairment of learning and memory in TAG-1 deficient mice associated with shorter CNS internodes and disrupted juxtaparanodes. Mol Cell Neurosci 39, 478-90.
- Stamatakis A, Pondiki S, Kitraki E, Diamantopoulou A, Panagiotaropoulos T, Raftogianni A, Stylianopoulou F. (2008). Effect of neonatal handling on adult rat spatial learning and memory following acute stress. Stress 11, 148-59.
- Manolis E, Fillipou D, Theocharis S, Panagiotaropoulos T, Lappas D, Mompheratou E. (2007). Anatomical landmarks: Dimensions of the mastoid air cell system in the Mediterranean population. Our experience from the anatomy of 298 temporal bones. Anat Sci Int 82, 139-146.
- Manolis EN, Kaklamanos IG, Spanakis N, Filippou DK, Panagiotaropoulos T, Tsakris A, Siomos K. (2007) Tissue concentration of transforming growth factor beta1 and basic fibroblast growth factor in skin wounds created with a CO2 laser and scalpel: a comparative experimental study, using an animal model of skin resurfacing. Wound Rep Regen 15, 252-7.
- Panagiotaropoulos T, Stylianopoulou F. (2006). Behavioral mechanisms and neurobiological substrate of frustration. Noesis, 2,105-121 (in greek).
- Garoflos E*, Panagiotaropoulos T*, Pondiki S, Stamatakis A, Philippidis H, Stylianopoulou F. (2005). Cellular mechanisms underlying the effects of an early experience on cognitive abilities and affective states. Ann Gen Psychiatry 4:8.
- Panagiotaropoulos T, Papaioannou A, Pondiki S, Prokopiou A, Stylianopoulou F, Gerozissis K. (2004). Effect of neonatal handling and sex on basal and chronic stress-induced corticosterone and leptin secretion. Neuroendocrinology 79:109-118.
- Panagiotaropoulos T, Pondiki S, Papaioannou A, Stamatakis A, Alikaridis F, Gerozissis K, Stylianopoulou F. (2004). Neonatal handling and gender modulate brain monoamines and plasma corticosterone levels following repeated stressors in adulthood. Neuroendocrinology 80, 181-191.
articles in preparation
- Panagiotaropoulos TI, Theodoni P, Kapoor V, Deco G, Logothetis N.K. Decorrelated discharge fluctuations in prefrontal microcircuits during visual consciousness.
- Panagiotaropoulos TI, Besserve M, Crocker B, Kapoor V, Tolias AS, Panzeri S, Logothetis NK. Beta oscillations propagate as traveling waves and convey visual information in the inferior convexity of the macaque prefrontal cortex.
- Besserve M, Crocker B, Kapoor V, Tolias AS, Panzeri S, Logothetis NK, Panagiotaropoulos TI. Identifying endogenous rhythmic spatio-temporal patterns in multielectrode array recordings.
- Crocker B, Kapoor V, Panzeri S, Logothetis NK, Panagiotaropoulos TI. An information-theoretic analysis of local field potentials and spiking activity in the inferior convexity of the macaque prefrontal cortex during anesthesia.
- Kapoor V, Logothetis NK, Panagiotaropoulos TI. Dissociation between rank order and conscious visual perception-specific neural signals in the macaque prefrontal cortex.
- Kapoor V, Logothetis NK, Panagiotaropoulos TI.Competitive interactions influence off responses in the macaque prefrontal cortex.
- Panagiotaropoulos TI, Logothetis NK. (2013) 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. Visual Perception of Shape, Space and Appearance. (Ed. L. Albertazzi). John Wiley & Sons Ltd.
- Panagiotaropoulos TI, Logothetis NK, Keliris GA. Neural approaches to perceptual organization. in The Handbook of Computational Perceptual Organization, Eds. Gepshtein-Maloney. (in press).
Selected Conference Abstracts
- Safavi S, Panagiotaropoulos TI, Kapoor V, Logothetis NK, Besserve M. Coupling between spiking activity and beta band spatiotemporal patterns in the macaque PFC. 43rd Annual Meeting of the Society for Neuroscience (Neuroscience 2013),San Diego, CA, USA.
- Panagiotaropoulos TI, Besserve M, Logothetis NK. (October 2012). Beta oscillations propagate as traveling waves in the macaque prefrontal cortex. 42nd Annual Meeting of the Society for Neuroscience (Neuroscience 2012),New Orleans, LA, USA.
- Theodoni P, Panagiotaropoulos TI, Kapoor V, Logothetis NK, Deco G. (July 2012). Cortical microcircuit dynamics in visual awareness. AREADNE Research in Encoding And Decoding of Neural Ensembles, Santorini, Greece.
- Besserve M, Panagiotaropoulos T, Crocker B, Kapoor V, Tolias AS, Panzeri S, Logothetis NK (March 2012). Identifying endogenous rhythmic spatiotemporal patterns in microelectrode array recordings, 9th Annual Computational and Systems Neuroscience Meeting. Salt Lake City, Utah, USA.
- Panagiotaropoulos TI, Besserve M, Crocker B, Kapoor V, Tolias AS, Panzeri S, Logothetis NK. (November 2011). Spatiotemporal mapping of rhythmic activity in the inferior convexity of the macaque prefrontal cortex. 41st Annual Meeting of the Society for Neuroscience (Neuroscience 2011), Washington, DC, USA.
- Crocker B, Kapoor V, Panzeri S, Logothetis NK, Panagiotaropoulos T. (November 2011). Low frequency local field potentials in the inferior convexity of the macaque prefrontal cortex convey visual information during anesthesia. 41st Annual Meeting of the Society for Neuroscience (Neuroscience 2011), Washington, DC, USA.
- Panagiotaropoulos T, Kapoor V, Logothetis NK. (June 2010). Reduction of Correlated Noise in the Macaque Prefrontal Cortex during Conscious Visual Perception. AREADNE Research in Encoding And Decoding of Neural Ensembles, Santorini, Greece.
- Panagiotaropoulos T, Komlos M, Kapoor V, Logothetis NK (Octover 2009). Dynamical changes in functional circuitry of the macaque prefrontal cortex mediating a perceptual switch. 39th Annual Meeting of the Society for Neuroscience (Neuroscience 2009), Chicago, IL, USA.
- Panagiotaropoulos T, Kapoor V, Keliris GA, Tolias AS, Logothetis NK. (July 2008) Neurophysiological substrates of visual awareness in the macaque prefrontal cortex. Forum of European Neuroscience, Geneva, Switzerland.
- Panagiotaropoulos T., Kapoor V., Keliris G.A., Tolias A.S., Logothetis N.K. (July 2008). Single units reflect visual awareness in the macaque prefrontal cortex. AREADNE Research in Encoding And Decoding of Neural Ensembles, Santorini, Greece.
- Schmidt M.C, Panagiotaropoulos T., Augath M.A., Logothetis N.K., Smirnakis S.M. (November 2007). Areas V2 and V3 remain active and retinotopically organized in the absence of direct V1 input. 37th Annual Meeting of the Society for Neuroscience (Neuroscience 2007), San Diego, California, U.S.A.
- Tolias AS, Ecker A, Keliris GA, Panagiotaropoulos T, Panzeri S, Logothetis NK. (September 2007). Population codes, correlations and coding uncertainty. Neural Coding, Computation and Dynamics (NCCD),Hossegor, France.
- Panagiotaropoulos T, Karagogeos D, Watanabe K, Stylianopoulou F. (July 2004). Spatial learning and locomotor deficits in TAG-1 male and female knockout mice. Forum of European Neuroscience, Lisbon, Portugal.
- Panagiotaropoulos T, Stylianopoulou F. (May 2002). Frustration of maternal contact in neonatal rats affects their ability for spatial navigation during adulthood. EURESCO, Neural Mechanisms of Learning and Memory, Evian, France.
June 2014 Oxford University, Oxford, U.K.
April 2014 Newcastle University, Newcastle, U.K.
November 2013 California Institute of Technology, Pasadena, U.S.A
January 2013 University of Tübingen, Tübingen, Germany
January 2013 University of Sussex, Sussex, U.K.
October 2012 Society for Neuroscience Meeting, New Orleans, U.S.A
January 2012 Universitat Pompeu Fabra, Barcelona, Spain.
September 2008 Universitat Pompeu Fabra, Barcelona, Spain.
June 2005 University of Crete, Heraklion, Greece.
?ay 2003 9th Pan-Hellenic Conference of Psychology, Rhodes, Greece.
March 2001 21st European Winter Conference on Brain Research, Arc 1800, France.
2006-2012 Max Planck Society Postdoctoral fellowship.
2009 FENS travel award (for participation in the annual meeting of the Society for Neuroscience)
2006 DAAD (Deutscher Akademischer Austauschdienst)
Research grant Enhancement of plasticity of primary visual cortex following retinal lesions.
2003-2006 Greek State Scholarships Foundation
Phd scholarship in Neuroscience
2003 Aristotle award for the best submitted paper: Cellular mechanisms underlying the effects of an early experience on cognitive abilities and affective states. 1st International Congress on Brain and Behavior, Thessaloniki, Greece.
2003 The Vivian Smith Advanced Studies Institute of the International Neuropsychological Society. Travel Award for participation in the Summer Institute: Memory and the Amnesias. Xylokastro, Greece.
2002-2005 National & Kapodistrian University of Athens, Research Grant Iraklitos: The effect of frustration of maternal contact on the cognitive function of the rat: Psychobiological mechanisms.
2002 ESF-EURESCO Travel grant for participation in the European Research Conference on Neural Mechanisms of Learning and Memory, Evian, France.
2002 EUROSTERONE Travel grant for participation in the Summer School: Neurobiology of Stress in Health and Disease, Elba, Italy.
2001 Vergina award for the best submitted paper. Interaction between an early experience and gonadal hormones in determining the adaptability of the organism. 1st Congress of the Hellenic Association of Psychophysiology, Thessaloniki, Greece.
2001 Research Grant from French government (Program Platon, dossier No 20012517). Laboratoire Physiopathologie de la Nutrition, Universite Paris VII, CNRS ESA 7059.
Frontiers in Human Neuroscience (Associate Editor)
Ad Hoc Reviewer
Neuron, Current Biology, Philosophical Transactions of the Royal Society B: Biological Sciences, Frontiers in Human Neuroscience, Frontiers in Physiology,
Frontiers in Psychology, Annals of Biomedical Engineering, BBSRC
Society for Neuroscience (SfN)
Federation of the European Neuroscience Societies (FENS)
Hellenic Society for Neurosciences (HSFN)
2002-2005 Teaching assistant Graduate Program in Cognitive Science University of Athens (Prof. Fotini Stylianopoulou)
(Cognitive Neuroscience, Neural mechanisms of learning and memory)
2012-present Shervin Shafavi Master Thesis Student
2008-present Vishal Kapoor PhD student (MPI for Biological Cybernetics)
2011-2012 Shervin Shafavi, Sumit Pai, Manuel Alejandro Torres - Lab rotation students
2009-2011 Britni Crocker Master Thesis Student (now PhD student - MIT)