Saccades during visual exploration align hippocampal 3–8 Hz rhythms in human and non-human primates

Visual exploration in primates depends on saccadic eye movements (SEMs) that cause alternations of neural suppression and enhancement. This modulation extends beyond retinotopic areas, and is thought to facilitate perception; yet saccades may also influence brain regions critical for forming memories of these exploratory episodes. The hippocampus, for example, shows oscillatory activity that is generally associated with encoding of information. Whether or how hippocampal oscillations are influenced by eye movements is unknown. We recorded the neural activity in the human and macaque hippocampus during visual scene search. Across species, SEMs were associated with a time-limited alignment of a low-frequency (3–8 Hz) rhythm. The phase alignment depended on the task and not only on eye movements per se, and the frequency band was not a direct consequence of saccade rate. Hippocampal theta-frequency oscillations are produced by other mammals during repetitive exploratory behaviors, including whisking, sniffing, echolocation, and locomotion. The present results may reflect a similar yet distinct primate homologue supporting active perception during exploration.

[1]  Steven F. Kalik,et al.  Analysis of perisaccadic field potentials in the occipitotemporal pathway during active vision. , 2003, Journal of neurophysiology.

[2]  A. Treves,et al.  Theta-paced flickering between place-cell maps in the hippocampus , 2011, Nature.

[3]  M. Shapiro,et al.  Bidirectional changes to hippocampal theta–gamma comodulation predict memory for recent spatial episodes , 2010, Proceedings of the National Academy of Sciences.

[4]  D. Burr,et al.  Selective suppression of the magnocellular visual pathway during saccadic eye movements , 1994, Nature.

[5]  Michael R Ibbotson,et al.  Direction and contrast tuning of macaque MSTd neurons during saccades. , 2009, Journal of neurophysiology.

[6]  K. Hoffmann,et al.  Neural Dynamics of Saccadic Suppression , 2009, Journal of Neuroscience.

[7]  Michael R. Ibbotson,et al.  Saccadic Modulation of Neural Responses: Possible Roles in Saccadic Suppression, Enhancement, and Time Compression , 2008, The Journal of Neuroscience.

[8]  Michael J. Jutras,et al.  Oscillatory activity in the monkey hippocampus during visual exploration and memory formation , 2013, Proceedings of the National Academy of Sciences.

[9]  M. Kahana,et al.  Reset of human neocortical oscillations during a working memory task , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  N. Ulanovsky,et al.  Hippocampal cellular and network activity in freely moving echolocating bats , 2007, Nature Neuroscience.

[11]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[12]  K. Hoffmann,et al.  Neural Mechanisms of Saccadic Suppression , 2002, Science.

[13]  T. Sejnowski,et al.  Learning where to look for a hidden target , 2013, Proceedings of the National Academy of Sciences.

[14]  長澤 哲郎 Occipital gamma-oscillations modulated during eye movement tasks : simultaneous eye tracking and electrocorticography recording in epileptic patients , 2013 .

[15]  O. Vinogradova Expression, control, and probable functional significance of the neuronal theta-rhythm , 1995, Progress in Neurobiology.

[16]  C. H. Vanderwolf,et al.  Hippocampal electrical activity and voluntary movement in the rat. , 1969, Electroencephalography and clinical neurophysiology.

[17]  Nicolas Brunel,et al.  Sensory neural codes using multiplexed temporal scales , 2010, Trends in Neurosciences.

[18]  J L Ringo,et al.  Activity linked to externally cued saccades in single units recorded from hippocampal, parahippocampal, and inferotemporal areas of macaques. , 1997, Journal of neurophysiology.

[19]  B. Givens Stimulus‐evoked resetting of the dentate theta rhythm: relation to working memory , 1996, Neuroreport.

[20]  E. Grastyán,et al.  Hippocampal electrical activity during the development of conditioned reflexes. , 1959, Electroencephalography and clinical neurophysiology.

[21]  Sonja Grün,et al.  Cross-frequency interaction of the eye-movement related LFP signals in V1 of freely viewing monkeys , 2012, Front. Syst. Neurosci..

[22]  Martin Vinck,et al.  The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization , 2010, NeuroImage.

[23]  Adriano B. L. Tort,et al.  Theta–gamma coupling increases during the learning of item–context associations , 2009, Proceedings of the National Academy of Sciences.

[24]  D. Hubel,et al.  Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys , 2000, Nature Neuroscience.

[25]  Kari L Hoffman,et al.  Saccades during Object Viewing Modulate Oscillatory Phase in the Superior Temporal Sulcus , 2011, The Journal of Neuroscience.

[26]  Ramona O. Hopkins,et al.  Experience-Dependent Eye Movements, Awareness, and Hippocampus-Dependent Memory , 2006, The Journal of Neuroscience.

[27]  Joseph H. Goldberg,et al.  Identifying fixations and saccades in eye-tracking protocols , 2000, ETRA.

[28]  Hjalmar K Turesson,et al.  Category-selective phase coding in the superior temporal sulcus , 2012, Proceedings of the National Academy of Sciences.

[29]  E. Garcı́a-Austt,et al.  Reset of hippocampal rhythmical activities by afferent stimulation , 1978, Brain Research Bulletin.

[30]  Peter Lakatos,et al.  Dynamics of Active Sensing and perceptual selection , 2010, Current Opinion in Neurobiology.

[31]  Stefan Everling,et al.  A long-range fronto-parietal 5- to 10-Hz network predicts "top-down" controlled guidance in a task-switch paradigm. , 2014, Cerebral cortex.

[32]  Neil Burgess,et al.  The theta rhythm , 2005, Hippocampus.

[33]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

[34]  L. P. O'Keefe,et al.  The influence of fixational eye movements on the response of neurons in area MT of the macaque , 1998, Visual Neuroscience.

[35]  Conrado A. Bosman,et al.  Functional differences of low- and high-frequency oscillatory dynamics during illusory border perception , 2010, Brain Research.

[36]  Caspar M. Schwiedrzik,et al.  (Micro)Saccades, corollary activity and cortical oscillations , 2009, Trends in Cognitive Sciences.

[37]  G. Buzsáki,et al.  Spike phase precession persists after transient intrahippocampal perturbation , 2005, Nature Neuroscience.

[38]  Nikos K. Logothetis,et al.  Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex , 1998, Experimental Brain Research.

[39]  W. Singer,et al.  Synchronization of neuronal responses in primary visual cortex of monkeys viewing natural images. , 2008, Journal of neurophysiology.

[40]  Christopher K. Kovach,et al.  Manifestation of ocular-muscle EMG contamination in human intracranial recordings , 2011, NeuroImage.

[41]  G. Buzsáki Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory , 2005, Hippocampus.

[42]  Sonja Grün,et al.  Saccade-Related Modulations of Neuronal Excitability Support Synchrony of Visually Elicited Spikes , 2011, Cerebral cortex.

[43]  R. Reid,et al.  Saccadic Eye Movements Modulate Visual Responses in the Lateral Geniculate Nucleus , 2002, Neuron.

[44]  P. Latour Visual threshold during eye movements , 1962 .

[45]  Michael R. Ibbotson,et al.  Effects of saccades on visual processing in primate MSTd , 2010, Vision Research.

[46]  Gustavo Deco,et al.  Oscillations, Phase-of-Firing Coding, and Spike Timing-Dependent Plasticity: An Efficient Learning Scheme , 2009, The Journal of Neuroscience.

[47]  Neal J Cohen,et al.  The nature of change detection and online representations of scenes. , 2004, Journal of experimental psychology. Human perception and performance.

[48]  M. Hasselmo What is the function of hippocampal theta rhythm?—Linking behavioral data to phasic properties of field potential and unit recording data , 2005, Hippocampus.

[49]  W. Singer,et al.  Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle , 2012, Proceedings of the National Academy of Sciences.

[50]  Eishi Asano,et al.  Human occipital cortices differentially exert saccadic suppression: Intracranial recording in children , 2013, NeuroImage.

[51]  P. Fries,et al.  Gamma-Band Synchronization in the Macaque Hippocampus and Memory Formation , 2009, The Journal of Neuroscience.

[52]  M. Ibbotson,et al.  Visual perception and saccadic eye movements , 2011, Current Opinion in Neurobiology.

[53]  I. Nelken,et al.  Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades , 2008, Neuron.

[54]  J. Lisman,et al.  The Theta-Gamma Neural Code , 2013, Neuron.

[55]  Is the functional connectivity within temporal lobe influenced by saccadic eye movements? , 2002, Journal of neurophysiology.

[56]  J L Ringo,et al.  Eye movements modulate activity in hippocampal, parahippocampal, and inferotemporal neurons. , 1994, Journal of neurophysiology.

[57]  G. Karmos,et al.  Transient cortical excitation at the onset of visual fixation. , 2008, Cerebral cortex.

[58]  M. Ibbotson,et al.  Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex. , 2006, Cerebral cortex.

[59]  U. Rutishauser,et al.  Human memory strength is predicted by theta-frequency phase-locking of single neurons , 2010, Nature.

[60]  J. Fell,et al.  Declarative memory formation in hippocampal sclerosis: an intracranial event-related potentials study , 2007, Neuroreport.

[61]  M. Kahana,et al.  Synchronous and Asynchronous Theta and Gamma Activity during Episodic Memory Formation , 2013, The Journal of Neuroscience.

[62]  Pascal Fries,et al.  A Microsaccadic Rhythm Modulates Gamma-Band Synchronization and Behavior , 2009, The Journal of Neuroscience.

[63]  J. Fell,et al.  Phase/amplitude reset and theta–gamma interaction in the human medial temporal lobe during a continuous word recognition memory task , 2005, Hippocampus.

[64]  B. McNaughton,et al.  EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. , 2007, Journal of neurophysiology.