Functional Specialization within the Medial Frontal Gyrus for Perceptual Go/No-Go Decisions Based on What, When, and Where Related Information: An fMRI Study

Cortical systems engaged during executive and volitional functions receive and integrate input from multiple systems. However, these integration processes are not well understood. In particular, it is not known whether these input pathways converge or remain segregated at the executive levels of cortical information processing. If unilateral information streams are conserved within structures that serve high-level executive functions, then the functional organization within these structures would predictably be similarly organized. If, however, unilateral input information streams are integrated within executive-related structures, then activity patterns will not necessarily reflect lower organizations. In this study, subjects were imaged during the performance of a perceptual go/nogo task for which instructions were based on spatial (where), temporal (when), or object (what) stimulus features known to engage unilateral processing streams, and the expected hemispheric biases were observed for early processing areas. For example, activity within the inferior and middle occipital gyri, and the middle temporal gyrus, during the what and when tasks, was biased toward the left hemisphere, and toward the right hemisphere during the where task. We discover a similar lateralization within the medial frontal gyrus, a region associated with high-level executive functions and decision-related processes. This lateralization was observed regardless of whether the response was executed or imagined, and was demonstrated in multiple sensory modalities. Although active during the go/no-go task, the cingulate gyrus did not show a similar lateralization. These findings further differentiate the organizations and functions of the medial frontal and cingulate executive regions, and suggest that the executive mechanisms operative within the medial frontal gyrus preserve fundamental aspects of input processing streams.

[1]  E. Warrington.  Neuropsychological studies of object recognition. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[2]  S Clare,et al.  Functional magnetic resonance imaging of single motor events reveals human presupplementary motor area , 1997, Annals of neurology.

[3]  Apostolos P Georgopoulos,et al.  Neural aspects of cognitive motor control , 2000, Current Opinion in Neurobiology.

[4]  Carlo Miniussi,et al.  Watching where you look: modulation of visual processing of foveal stimuli by spatial attention , 2002, Neuropsychologia.

[5]  R. Coghill,et al.  Hemispheric lateralization of somatosensory processing. , 2001, Journal of neurophysiology.

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

[7]  E. Renzi,et al.  Spatial Memory and Hemispheric Locus of Lesion , 1977, Cortex.

[8]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

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

[10]  C. Olson,et al.  Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. , 1992, Cerebral cortex.

[11]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[12]  Hiroshi Fukuda,et al.  The human prefrontal and parietal association cortices are involved in NO-GO performances—an event-related fMRI study , 2000, NeuroImage.

[13]  Sebastiano Bagnara,et al.  Laterality effects for simple and complex geometrical figures, and nonsense patterns , 1978, Neuropsychologia.

[14]  Leslie G. Ungerleider,et al.  Dissociation of object and spatial visual processing pathways in human extrastriate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Hirsch,et al.  Concordance between Functional Magnetic Resonance Imaging and Intraoperative Language Mapping , 2000, Stereotactic and Functional Neurosurgery.

[16]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[17]  J L Rapoport,et al.  The role of the anterior cingulate in automatic and controlled processes: a developmental neuroanatomical study. , 1997, Developmental psychobiology.

[18]  M. Coltheart.  Hemispheric asymmetry , 1978, Nature.

[19]  R. Dolan,et al.  Active representation of shape and spatial location in man. , 1996, Cerebral cortex.

[20]  J. Driver,et al.  Crossmodal links in endogenous and exogenous spatial attention: evidence from event-related brain potential studies , 2001, Neuroscience & Biobehavioral Reviews.

[21]  P. Goldman-Rakic,et al.  Interhemispheric integration: I. Symmetry and convergence of the corticocortical connections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) in the rhesus monkey. , 1991, Cerebral cortex.

[22]  Katherine J. Alcock,et al.  Pitch and Timing Abilities in Adult Left-Hemisphere-Dysphasic and Right-Hemisphere-Damaged Subjects , 2000, Brain and Language.

[23]  J. Hirsch,et al.  An Integrated Functional Magnetic Resonance Imaging Procedure for Preoperative Mapping of Cortical Areas Associated with Tactile, Motor, Language, and Visual Functions , 2000, Neurosurgery.

[24]  Michael Erb,et al.  Sequential activation of supplementary motor area and primary motor cortex during self-paced finger movement in human evaluated by functional MRI , 1997, Neuroscience Letters.

[25]  Giacomo Rizzolatti,et al.  Right hemisphere superiority for programming oculomotion: Evidence from simple reaction time experiments , 1988, Neuropsychologia.

[26]  J Tanji,et al.  Comparison of neuronal activity in the supplementary motor area and primary motor cortex. , 1996, Brain research. Cognitive brain research.

[27]  Timothy Edward John Behrens,et al.  Functional Asymmetry for Auditory Processing in Human Primary Auditory Cortex , 2003, The Journal of Neuroscience.

[28]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[29]  E. Renzi,et al.  Constructional Apraxia and Hemispheric Locus of Lesion , 1964 .

[30]  Scott T. Grafton,et al.  Human functional anatomy of visually guided finger movements. , 1992, Brain : a journal of neurology.

[31]  Leslie G. Ungerleider,et al.  Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys , 1982, Behavioural Brain Research.

[32]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Gian Luca Romani,et al.  “What” versus “Where” in the audiovisual domain: An fMRI study , 2006, NeuroImage.

[34]  Ravi S. Menon,et al.  Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. , 1993, Biophysical journal.

[35]  J. Tanji,et al.  A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: neuronal activity during a learned motor task. , 1992, Journal of neurophysiology.

[36]  C D Salzman,et al.  Neural mechanisms for forming a perceptual decision. , 1994, Science.

[37]  K. Kiehl,et al.  Event‐related fMRI study of response inhibition , 2001, Human brain mapping.

[38]  R. Zatorre,et al.  Right temporal cortex is critical for utilization of melodic contextual cues in a pitch constancy task. , 2004, Brain : a journal of neurology.

[39]  A. Turken,et al.  Dissociation between conflict detection and error monitoring in the human anterior cingulate cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[40]  J. Mazziotta,et al.  MRI‐PET Registration with Automated Algorithm , 1993, Journal of computer assisted tomography.

[41]  M. Baulac,et al.  Cerebral Substrates for Musical Temporal Processes , 2001, Annals of the New York Academy of Sciences.

[42]  P. Roland,et al.  Supplementary motor area and other cortical areas in organization of voluntary movements in man. , 1980, Journal of neurophysiology.

[43]  R. Mccarthy,et al.  The dissolution of semantics , 1990, Nature.

[44]  D. V. von Cramon,et al.  Error Monitoring Using External Feedback: Specific Roles of the Habenular Complex, the Reward System, and the Cingulate Motor Area Revealed by Functional Magnetic Resonance Imaging , 2003, The Journal of Neuroscience.

[45]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[46]  K. A. Hadland,et al.  The Effect of Cingulate Cortex Lesions on Task Switching and Working Memory , 2003, Journal of Cognitive Neuroscience.

[47]  B. J. Casey,et al.  The Effect of Preceding Context on Inhibition: An Event-Related fMRI Study , 2002, NeuroImage.

[48]  J. A. Frost,et al.  Somatotopic mapping of the human primary motor cortex with functional magnetic resonance imaging , 1995, Neurology.

[49]  Ruth Ann Atchley,et al.  Hemispheric specialization in the detection of subjective objects , 1998, Neuropsychologia.

[50]  P. Goldman-Rakic,et al.  Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. , 1996, Cerebral cortex.

[51]  G. Lindinger,et al.  Supplementary Motor Area Activation Preceding Voluntary Movement Is Detectable with a Whole-Scalp Magnetoencephalography System , 2000, NeuroImage.

[52]  R. Klein,et al.  A review of the evidence for a disengage deficit following parietal lobe damage , 2001, Neuroscience & Biobehavioral Reviews.

[53]  R. Zatorre.  Neural Specializations for Tonal Processing , 2001, Annals of the New York Academy of Sciences.

[54]  D S Goodin,et al.  The Decision to Make a Movement: Neurophysiological Insights , 1997, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[55]  R. C. Oldfield.  THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[56]  P. B. Cipolloni,et al.  Cortical connections of the frontoparietal opercular areas in the Rhesus monkey , 1999, The Journal of comparative neurology.

[57]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[58]  E. Phelps,et al.  FMRI of the prefrontal cortex during overt verbal fluency , 1997, Neuroreport.

[59]  Joy Hirsch,et al.  Interconnected Large-Scale Systems for Three Fundamental Cognitive Tasks Revealed by Functional MRI , 2001, Journal of Cognitive Neuroscience.

[60]  S. Hofman.  Common hemisphericity of language and music in a musician: a case report , 1998 .

[61]  H. Garavan,et al.  Dissociable Executive Functions in the Dynamic Control of Behavior: Inhibition, Error Detection, and Correction , 2002, NeuroImage.

[62]  A. Cowey,et al.  A distortion of perceived space in patients withright-hemisphere lesions and visual hemineglect , 1999, Neuropsychologia.

[63]  M. D’Esposito,et al.  Neural Evidence for Representation-Specific Response Selection , 2003, Journal of Cognitive Neuroscience.

[64]  Y. Miyashita,et al.  Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. , 1999, Brain : a journal of neurology.

[65]  Joy Hirsch,et al.  Cortical reorganization following intradigital tendon transfer , 2006, Neuroreport.

[66]  P. Goldman-Rakic,et al.  Interhemispheric integration: II. Symmetry and convergence of the corticostriatal projections of the left and the right principal sulcus (PS) and the left and the right supplementary motor area (SMA) of the rhesus monkey. , 1991, Cerebral cortex.

[67]  P S Goldman-Rakic,et al.  Circuitry of the frontal association cortex and its relevance to dementia. , 1987, Archives of gerontology and geriatrics.

[68]  S. Rauch,et al.  Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and the counting stroop , 1999, Biological Psychiatry.