Preparing hearts and minds: cardiac slowing and a cortical inhibitory network.

Preparing for a cued, speeded response induces a set of physiological changes. A review of the psychophysiology of preparation suggested that inhibition of action was an important process among the constellation of changes constituting attentive preparation. The current experiment combined event-related functional magnetic resonance imaging and cardiac inter-beat interval measures in an experiment that compared preparing for a response, watching stimuli without responding, and responding in the absence of preparation. Ten college-aged participants were tested in an initial psychophysiological experiment followed by two scanning sessions during which reverse spiral imaging was performed concurrent with inter-beat interval measurement. Two analytic approaches were used to confirm blood oxygenation level dependent responses during preparation, and these converged to show inferior prefrontal and related subthalamic nuclei activity in the context of other known changes related to brain attentional networks. Subthalamic nuclei changes were related to the depth of preparatory cardiac deceleration. This pattern of findings suggests that preparation involves the activation of a complex inhibitory neural network implicating brain and autonomic nervous systems.

[1]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[2]  J. Cohen,et al.  Spiral K‐space MR imaging of cortical activation , 1995, Journal of magnetic resonance imaging : JMRI.

[3]  J. Jennings,et al.  Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: Implications for the cortical and subcortical regulation of cardiac autonomic activity. , 2004, Psychophysiology.

[4]  M. Posner,et al.  Pathologies of brain attentional networks , 2000, Neuroscience & Biobehavioral Reviews.

[5]  Maurits W. van der Molen,et al.  Cardiac timing and the central regulation of action , 2002, Psychological research.

[6]  B. J. Yates,et al.  Integration of somatic and visceral inputs by the brainstem Functional considerations , 1998, Experimental Brain Research.

[7]  Michael Erb,et al.  Separation of phasic arousal and expectancy effects in a speeded reaction time task via fMRI. , 2009, Psychophysiology.

[8]  H Johansen-Berg,et al.  Towards an understanding of gait control: brain activation during the anticipation, preparation and execution of foot movements , 2004, NeuroImage.

[9]  Geert J. M. van Boxtel,et al.  Stimulation of the Subthalamic Region Facilitates the Selection and Inhibition of Motor Responses in Parkinson's Disease , 2006, Journal of Cognitive Neuroscience.

[10]  J. May,et al.  Is There a Functional Neural Correlate of Individual Differences in Cardiovascular Reactivity? , 2005, Psychosomatic medicine.

[11]  G. Logan,et al.  Converging Evidence for a Fronto-Basal-Ganglia Network for Inhibitory Control of Action and Cognition , 2007, The Journal of Neuroscience.

[12]  Adam R. Aron,et al.  Progress in Executive-Function Research , 2008 .

[13]  A. MacDonald,et al.  Effects of varying the experimental design of a cognitive control paradigm on behavioral and functional imaging outcome measures , 2008 .

[14]  Bob S. Hu,et al.  Fast Spiral Coronary Artery Imaging , 1992, Magnetic resonance in medicine.

[15]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[16]  E. Neafsey,et al.  Prefrontal cortical control of the autonomic nervous system: anatomical and physiological observations. , 1990, Progress in brain research.

[17]  Jonathan S. Cant,et al.  Effector-specific fields for motor preparation in the human frontal cortex , 2007, NeuroImage.

[18]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

[19]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[20]  A. Nobre,et al.  Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts , 2000, Neuropsychologia.

[21]  M. W. van der Molen,et al.  On the synchrony of stopping motor responses and delaying heartbeats. , 1992, Journal of experimental psychology. Human perception and performance.

[22]  P. Obrist,et al.  Presidential Address, 1975. The cardiovascular-behavioral interaction--as it appears today. , 1976, Psychophysiology.

[23]  E. Aarts,et al.  Anticipatory activity in anterior cingulate cortex can be independent of conflict and error likelihood. , 2008, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[25]  Richard S. Frackowiak,et al.  A bilateral cortico-bulbar network associated with breath holding in humans, determined by functional magnetic resonance imaging , 2008, NeuroImage.

[26]  Philipp Kanske,et al.  Probing the Mechanisms of Attention , 2007 .

[27]  A. Nobre,et al.  The noradrenergic alpha2 agonist clonidine modulates behavioural and neuroanatomical correlates of human attentional orienting and alerting. , 2001, Cerebral cortex.

[28]  M. Woldorff,et al.  Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. , 2004, Cerebral cortex.

[29]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[30]  Anna C Nobre,et al.  Neural modulation by regularity and passage of time. , 2008, Journal of neurophysiology.

[31]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[32]  J. Tecce Contingent negative variation (CNV) and psychological processes in man. , 1972, Psychological bulletin.

[33]  C. Brunia Neural aspects of anticipatory behavior. , 1999, Acta psychologica.

[34]  T. Tsukamoto,et al.  Activation of insular cortex and subcortical regions related to feedback stimuli in a time estimation task: An fMRI study , 2006, Neuroscience Letters.

[35]  A. Nobre,et al.  The hazards of time , 2007, Current Opinion in Neurobiology.

[36]  Leslie G. Ungerleider,et al.  A neural system for human visual working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[38]  Bruce D. McCandliss,et al.  Response Anticipation and Response Conflict: An Event-Related Potential and Functional Magnetic Resonance Imaging Study , 2007, The Journal of Neuroscience.

[39]  Jin Fan,et al.  The activation of attentional networks , 2005, NeuroImage.

[40]  Stewart H. Mostofsky,et al.  Response Inhibition and Response Selection: Two Sides of the Same Coin , 2008, Journal of Cognitive Neuroscience.

[41]  Peter J Gianaros,et al.  Anterior cingulate activity correlates with blood pressure during stress. , 2005, Psychophysiology.

[42]  M. Rushworth Intention, Choice, and the Medial Frontal Cortex , 2008, Annals of the New York Academy of Sciences.

[43]  William L Miller,et al.  Transient and sustained brain activity during anticipatory visuospatial attention , 2008, Neuroreport.

[44]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[45]  Vince D. Calhoun,et al.  Functional neural networks underlying response inhibition in adolescents and adults , 2007, Behavioural Brain Research.

[46]  L. Swanson Cerebral hemisphere regulation of motivated behavior 1 1 Published on the World Wide Web on 2 November 2000. , 2000, Brain Research.

[47]  T. Shallice,et al.  The multiple dimensions of sustained attention , 2008, Cortex.

[48]  Maurits W van der Molen,et al.  Preparation for speeded action as a psychophysiological concept. , 2005, Psychological bulletin.

[49]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[50]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[51]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.