Role of the supplementary motor area during reproduction of supra-second time intervals: An intracerebral EEG study

ABSTRACT The supplementary motor area (SMA) has been shown to be involved in interval timing but its precise role remains a matter of debate. The present study was aimed at examining, by means of intracerebral EEG recordings, the time course of the activity in this structure, as well as in other functionally connected cortical (frontal, cingulate, insular and temporal) areas, during a visual time reproduction task. Four patients undergoing stereo‐electroencephalography (SEEG) for presurgical investigation of refractory focal epilepsy were enrolled. They were selected on the presence of depth electrodes implanted within the SMA. They were instructed to encode, keep in memory and then reproduce the duration (3, 5 and 7s) of emotionally‐neutral or negative pictures. Emotional stimuli were used with the aim of examining neural correlates of temporal distortions induced by emotion. Event‐related potentials (ERPs) were analyzed during three periods: During and at the extinction of the target interval (TI) and at the beginning of the reproduction interval (RI). Electrophysiological data revealed an ERP time‐locked to TI‐offset whose amplitude varied monotonically with TI‐duration. This effect was observed in three out of the four patients, especially within the SMA and the insula. It also involved the middle and anterior cingulate cortex, the superior, middle and inferior frontal gyri and the paracentral lobule. These effects were modulated by the prior TI‐duration and predicted variations in temporal reproduction accuracy. In contrast, modulations of ERPs with TI‐duration, emotion or temporal performance during the target or the reproduction interval were modest and less consistent across patients. These results demonstrate that, during reproduction of supra‐second time intervals, the SMA, in concert with a fronto‐insular network, is involved at the end of the target interval, and suggest a role in the duration categorization and decision making operations or alternatively in the preparedness of the timing of the future movement that will be executed during the reproduction phase.

[1]  R. Miall,et al.  Brain activation patterns during measurement of sub- and supra-second intervals , 2003, Neuropsychologia.

[2]  J. Coull.  Neural Substrates of Mounting Temporal Expectation , 2009, PLoS biology.

[3]  G. Pfurtscheller,et al.  Initiation of voluntary movements at free will and ongoing 0.1-Hz BOLD oscillations in the insula—a pilot study , 2014, Front. Integr. Neurosci..

[4]  A. Sanford,et al.  Slow potential correlates of preparatory set. , 1974, Biological psychology.

[5]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[6]  Katiuscia Sacco,et al.  Functional connectivity of the insula in the resting brain , 2011, NeuroImage.

[7]  Richard Ragot,et al.  Relationship between CNV and timing of an upcoming event , 2005, Neuroscience Letters.

[8]  Masahiko Inase,et al.  Striatal neurons encoded temporal information in duration discrimination task , 2008, Experimental Brain Research.

[9]  H. Coslett,et al.  Continuous Carryover of Temporal Context Dissociates Response Bias from Perceptual Influence for Duration , 2014, PloS one.

[10]  T. Nakada,et al.  Slow Accumulations of Neural Activities in Multiple Cortical Regions Precede Self-Initiation of Movement: An Event-Related fMRI Study , 2017, eNeuro.

[11]  R. Ivry,et al.  The neural representation of time , 2004, Current Opinion in Neurobiology.

[12]  D Akkal,et al.  Time predictability modulates pre-supplementary motor area neuronal activity , 2004, Neuroreport.

[13]  Franck Vidal,et al.  The CNV peak: an index of decision making and temporal memory. , 2003, Psychophysiology.

[14]  Martin Wiener,et al.  The image of time: A voxel-wise meta-analysis , 2010, NeuroImage.

[15]  David Ottoson,et al.  The Neural Basis of Perception , 1983 .

[16]  P. Lang.  International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[17]  Ann-Christine Ehlis,et al.  The time course of temporal discrimination: An ERP study , 2010, Clinical Neurophysiology.

[18]  R. Burgess,et al.  Connectivity of the frontal and anterior insular network: a cortico-cortical evoked potential study. , 2016, Journal of neurosurgery.

[19]  J. Talairach,et al.  Stereotaxic Approach to Epilepsy , 1973 .

[20]  G. Orban,et al.  Cortical Off Response Tuning for Stimulus Duration , 1996, Vision Research.

[21]  P. Montague,et al.  Ready…Go: Amplitude of the fMRI Signal Encodes Expectation of Cue Arrival Time , 2009, PLoS biology.

[22]  Hedderik van Rijn,et al.  Decoupling Interval Timing and Climbing Neural Activity: A Dissociation between CNV and N1P2 Amplitudes , 2014, The Journal of Neuroscience.

[23]  F. Vidal,et al.  Functional Anatomy of the Attentional Modulation of Time Estimation , 2004, Science.

[24]  Sylvie Droit-Volet,et al.  SMA Selectively Codes the Active Accumulation of Temporal, Not Spatial, Magnitude , 2015, Journal of Cognitive Neuroscience.

[25]  Aldo Genovesio,et al.  Feature- and Order-Based Timing Representations in the Frontal Cortex , 2009, Neuron.

[26]  Thomas H Rammsayer,et al.  Current-source density analysis of slow brain potentials during time estimation. , 2004, Psychophysiology.

[27]  Franck Vidal,et al.  Time processing reflected by EEG surface Laplacians , 2002, Experimental Brain Research.

[28]  Hugo Merchant,et al.  Information Processing in the Primate Basal Ganglia during Sensory-Guided and Internally Driven Rhythmic Tapping , 2014, The Journal of Neuroscience.

[29]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[30]  Hedderik van Rijn,et al.  Tonic and phasic dopamine fluctuations as reflected in beta-power predict interval timing behavior , 2014 .

[31]  Franck Vidal,et al.  When to act, or not to act: that's the SMA's question , 2016, Current Opinion in Behavioral Sciences.

[32]  Viviane Pouthas,et al.  ERPs in anterior and posterior regions associated with duration and size discriminations. , 2009, Neuropsychology.

[33]  Paul D. Kieffaber,et al.  The neural correlates of temporal judgments in the duration bisection task , 2013, Neuropsychologia.

[34]  Helga Lejeune,et al.  Vierordt's The Experimental Study of the Time Sense (1868) and its legacy , 2009 .

[35]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[36]  Warren H. Meck,et al.  Contingent negative variation and its relation to time estimation: a theoretical evaluation , 2011, Front. Integr. Neurosci..

[37]  J. Gibbon.  Scalar expectancy theory and Weber's law in animal timing. , 1977 .

[38]  Erich Schröger,et al.  Human auditory event-related potentials predict duration judgments , 2005, Neuroscience Letters.

[39]  Tadeusz W. Kononowicz,et al.  Slow Potentials in Time Estimation: The Role of Temporal Accumulation and Habituation , 2011, Front. Integr. Neurosci..

[40]  T Elbert,et al.  The processing of temporal intervals reflected by CNV-like brain potentials. , 1991, Psychophysiology.

[41]  Hugo Merchant,et al.  Neural basis for categorical boundaries in the primate pre-SMA during relative categorization of time intervals , 2018, Nature Communications.

[42]  J. Tanji,et al.  Interval time coding by neurons in the presupplementary and supplementary motor areas , 2009, Nature Neuroscience.

[43]  Anjan Chatterjee,et al.  Carving the clock at its component joints: neural bases for interval timing. , 2010, Journal of neurophysiology.

[44]  Daniel M. Corcos,et al.  Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis , 2006, NeuroImage.

[45]  John Wearden,et al.  Making decisions about time: Event-related potentials and judgements about the equality of durations , 2011, Biological Psychology.

[46]  Emotional modulation of attention affects time perception: evidence from event-related potentials. , 2014, Acta psychologica.

[47]  Franck Vidal,et al.  Timing, Storage, and Comparison of Stimulus Duration Engage Discrete Anatomical Components of a Perceptual Timing Network , 2008, Journal of Cognitive Neuroscience.

[48]  Martin Wiener,et al.  Repetition enhancement and memory effects for duration , 2015, NeuroImage.

[49]  W. Meck,et al.  How emotions colour our perception of time , 2007, Trends in Cognitive Sciences.

[50]  Warren H. Meck,et al.  Timing and Time Perception : A Critical Review of Neural Timing Signatures Before, During, and After the To‐Be‐Timed Interval , 2018 .

[51]  H. Rijn,et al.  Neuroelectromagnetic signatures of the reproduction of supra-second durations , 2015, Neuropsychologia.

[52]  C. M Gómez,et al.  Preparatory visuo-motor cortical network of the contingent negative variation estimated by current density , 2003, NeuroImage.

[53]  Bruno Rossion,et al.  Right hemispheric dominance of visual phenomena evoked by intracerebral stimulation of the human visual cortex , 2014, Human brain mapping.

[54]  Jason Tipples,et al.  Neural Bases for Individual Differences in the Subjective Experience of Short Durations (Less than 2 Seconds) , 2013, PloS one.

[55]  Jonas Obleser,et al.  Supplementary motor area activations predict individual differences in temporal-change sensitivity and its illusory distortions , 2014, NeuroImage.

[56]  Emiliano Macaluso,et al.  Physiological correlates of subjective time: Evidence for the temporal accumulator hypothesis , 2011, NeuroImage.

[57]  Matthew B. Wall,et al.  Time perception: Manipulation of task difficulty dissociates clock functions from other cognitive demands , 2007, Neuropsychologia.

[58]  Hugo Merchant,et al.  Neural basis of the perception and estimation of time. , 2013, Annual review of neuroscience.

[59]  Laurent Hugueville,et al.  Neural network involved in time perception: An fMRI study comparing long and short interval estimation , 2005, Human brain mapping.

[60]  Björn Herrmann,et al.  Selective attention to temporal features on nested time scales. , 2015, Cerebral cortex.

[61]  Warren H. Meck,et al.  Oscillatory multiplexing of neural population codes for interval timing and working memory , 2015, Neuroscience & Biobehavioral Reviews.

[62]  Geraint Rees,et al.  Encoding of Temporal Probabilities in the Human Brain , 2010, The Journal of Neuroscience.

[63]  Michel Thiebaut de Schotten,et al.  Short frontal lobe connections of the human brain , 2012, Cortex.

[64]  Michela Sarlo,et al.  Automatic Temporal Expectancy: A High-Density Event-Related Potential Study , 2013, PloS one.

[65]  Franck Vidal,et al.  The supplementary motor area in motor and sensory timing: evidence from slow brain potential changes , 1999, Experimental Brain Research.

[66]  R. Duncan Luce,et al.  Response Times: Their Role in Inferring Elementary Mental Organization , 1986 .

[67]  Hedderik van Rijn,et al.  Single trial beta oscillations index time estimation , 2015, Neuropsychologia.

[68]  Yong Hao Soh,et al.  Duration Magnitude and Memory Resource Demand , 2009 .

[69]  K. Davis,et al.  Two systems of resting state connectivity between the insula and cingulate cortex , 2009, Human brain mapping.

[70]  Ryota Kanai,et al.  Frequency tuning for temporal perception and prediction , 2016, Current Opinion in Behavioral Sciences.

[71]  Martin P. Paulus,et al.  Accumulation of Neural Activity in the Posterior Insula Encodes the Passage of Time , 2008 .