Do cortical co-ripples bind lines, letters, words, meanings, strategy and action in reading? Summary : Widespread lexical, semantic, executive and response processing areas co-ripple and phase-lock when detecting target words.

High-frequency phase-locked oscillations have been hypothesized to facilitate integration (‘binding’) of information encoded across widespread cortical areas. Ripples (∼100ms long ∼90Hz oscillations) co-occur broadly in multiple states and locations, but have only been associated with memory replay. We tested whether cortico-cortical co-ripples subserve a general role in binding by recording intracranial EEG during reading. Co-rippling strongly increased to words versus consonant-strings in visual, wordform and semantic areas when letters are binding into words, and words to meaning. Similarly, co-ripples increased prior to correct responses between executive, response, wordform and semantic sites when word meanings are binding to instructions and response. These effects dissociated from non-oscillatory activation and memory reinstatement. Co-ripples were phase-locked at zero-lag, even at long distances, supporting a general role in cognitive binding.

[1]  W. Singer,et al.  A biology-inspired recurrent oscillator network for computations in high-dimensional state space , 2022, bioRxiv.

[2]  Jessica N. Kelemen,et al.  Learned Motor Patterns Are Replayed in Human Motor Cortex during Sleep , 2022, The Journal of Neuroscience.

[3]  T. Robbins,et al.  The role of prefrontal cortex in cognitive control and executive function , 2021, Neuropsychopharmacology.

[4]  W. Singer Recurrent dynamics in the cerebral cortex: Integration of sensory evidence with stored knowledge , 2021, Proceedings of the National Academy of Sciences.

[5]  B. Q. Rosen,et al.  Widespread ripples synchronize human cortical activity during sleep, waking, and memory recall , 2021, bioRxiv.

[6]  William E. Allen,et al.  Cortical Observation by Synchronous Multifocal Optical Sampling Reveals Widespread Population Encoding of Actions , 2020, Neuron.

[7]  Kareem A. Zaghloul,et al.  Replay of cortical spiking sequences during human memory retrieval , 2020, Science.

[8]  R. Malach,et al.  Hippocampal sharp-wave ripples linked to visual episodic recollection in humans , 2019, Science.

[9]  E. Halgren,et al.  Posterior Hippocampal Spindle Ripples Co-occur with Neocortical Theta Bursts and Downstates-Upstates, and Phase-Lock with Parietal Spindles during NREM Sleep in Humans , 2019, The Journal of Neuroscience.

[10]  E. Halgren,et al.  Coordination of Human Hippocampal Sharpwave Ripples during NREM Sleep with Cortical Theta Bursts, Spindles, Downstates, and Upstates , 2019, The Journal of Neuroscience.

[11]  Nicolas Brunel,et al.  Coupled ripple oscillations between the medial temporal lobe and neocortex retrieve human memory , 2019, Science.

[12]  Helen C. Barron,et al.  Repetition suppression: a means to index neural representations using BOLD? , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  M. Zugaro,et al.  Hippocampo-cortical coupling mediates memory consolidation during sleep , 2016, Nature Neuroscience.

[14]  G. Buzsáki Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning , 2015, Hippocampus.

[15]  B. Merker Cortical gamma oscillations: the functional key is activation, not cognition , 2013, Neuroscience & Biobehavioral Reviews.

[16]  Orrin Devinsky,et al.  Sequential then Interactive Processing of Letters and Words in the Left Fusiform Gyrus , 2012, Nature Communications.

[17]  Rutvik H. Desai,et al.  The neurobiology of semantic memory , 2011, Trends in Cognitive Sciences.

[18]  S. Dehaene,et al.  The unique role of the visual word form area in reading , 2011, Trends in Cognitive Sciences.

[19]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[20]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[21]  N F Rulkov,et al.  Effect of synaptic connectivity on long-range synchronization of fast cortical oscillations. , 2008, Journal of neurophysiology.

[22]  Anders M. Dale,et al.  N400-like Magnetoencephalography Responses Modulated by Semantic Context, Word Frequency, and Lexical Class in Sentences , 2002, NeuroImage.

[23]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[24]  A. Treisman Solutions to the Binding Problem Progress through Controversy and Convergence , 1999, Neuron.

[25]  A. Revonsuo,et al.  Binding and Consciousness , 1999, Consciousness and Cognition.

[26]  L R Squire,et al.  Amnesia, memory and brain systems. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  E. Halgren,et al.  Spatio-temporal stages in face and word processing. 2. Depth-recorded potentials in the human frontal and Rolandic cortices , 1994, Journal of Physiology-Paris.

[28]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[29]  Ch. von der Malsburg,et al.  A neural cocktail-party processor , 1986, Biological Cybernetics.

[30]  E. Halgren,et al.  Spatio-temporal stages in face and word processing. I. Depth-recorded potentials in the human occipital, temporal and parietal lobes [corrected]. , 1994, Journal of physiology, Paris.