The pontine-driven somatic gaze tract contributes to affective processing in humans

The relevance of subcortical structures for affective processing is not fully understood. Inspired by the gerbil retino-raphe pathway that has been shown to regulate affective behavior and previous human work showing that the pontine region is important for processing emotion, we asked whether well-established tracts in humans traveling between the eye and the brain stem contribute to functions beyond their conventionally understood roles. Here we report neuroimaging findings showing that optic chiasm-brain stem diffusivity predict responses reflecting perceived arousal and valence. Analyses of subsequent task-evoked connectivity further revealed that visual affective processing implicates the brain stem, particularly the pontine region at an early stage of the cascade, projecting to cortico-limbic regions in a feedforward manner. The optimal model implies that all intrinsic connections between the regions of interest are unidirectional and outwards from the pontine region. These findings suggest that affective processing implicates regions outside the cortico-limbic network. The involvement of a phylogenetically older locus in the pons that has consequences in oculomotor control may imply adaptive consequences of affect detection.

[1]  N. Makris,et al.  Decreased volume of left and total anterior insular lobule in schizophrenia , 2006, Schizophrenia Research.

[2]  G. Vandewalle,et al.  Light as a modulator of cognitive brain function , 2009, Trends in Cognitive Sciences.

[3]  Oury Monchi,et al.  Regional Brain Stem Atrophy in Idiopathic Parkinson's Disease Detected by Anatomical MRI , 2009, PloS one.

[4]  Karl J. Friston,et al.  Variational free energy and the Laplace approximation , 2007, NeuroImage.

[5]  嘉兵 佐藤,et al.  スナネズミ(Mongolian gerbil; Meriones unguiculatus) 卵管内における精子の分布と先体反応について , 1988 .

[6]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[7]  N. Hadjikhani,et al.  Seeing Fearful Body Expressions Activates the Fusiform Cortex and Amygdala , 2003, Current Biology.

[8]  P. Basser,et al.  Comprehensive approach for correction of motion and distortion in diffusion‐weighted MRI , 2004, Magnetic resonance in medicine.

[9]  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.

[10]  R. Snaith,et al.  The Hospital Anxiety and Depression Scale , 1983 .

[11]  John C. Mazziotta,et al.  A Probabilistic Atlas and Reference System for the Human Brain , 2001 .

[12]  Yoram Hirshfeld,et al.  for Probabilistic , 1999 .

[13]  E. Rolls The functions of the orbitofrontal cortex , 1999, Brain and Cognition.

[14]  Dag Aarsland,et al.  Neuropsychiatric symptoms in Parkinson's disease , 2009, Movement disorders : official journal of the Movement Disorder Society.

[15]  K. Lesch,et al.  Long story short: the serotonin transporter in emotion regulation and social cognition , 2007, Nature Neuroscience.

[16]  T. T. Haug,et al.  The validity of the Hospital Anxiety and Depression Scale. An updated literature review. , 2002, Journal of psychosomatic research.

[17]  S. Holland,et al.  Abnormal deactivation of the inferior frontal gyrus during implicit emotion processing in youth with bipolar disorder: attenuated by medication. , 2014, Journal of psychiatric research.

[18]  S. Rauch,et al.  Structural brain magnetic resonance imaging of limbic and thalamic volumes in pediatric bipolar disorder. , 2005, The American journal of psychiatry.

[19]  Antonio P. Strafella,et al.  Imaging biomarkers in Parkinson’s disease and Parkinsonian syndromes: current and emerging concepts , 2017, Translational Neurodegeneration.

[20]  Peter J. Lang,et al.  Gaze Patterns When Looking at Emotional Pictures: Motivationally Biased Attention , 2004 .

[21]  S. Rauch,et al.  Neurobiology of emotion perception I: the neural basis of normal emotion perception , 2003, Biological Psychiatry.

[22]  Martin A Giese,et al.  Common neural correlates of emotion perception in humans , 2015, Human brain mapping.

[23]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[24]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[25]  Paul Kennedy,et al.  A preliminary psychometric evaluation of the Hospital Anxiety and Depression Scale (HADS) in 963 people livingwith a spinal cord injury , 2006, Psychology, health & medicine.

[26]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[27]  R. Levenson,et al.  Cultures of moderation and expression: emotional experience, behavior, and physiology in Chinese Americans and Mexican Americans. , 2005, Emotion.

[28]  P. Ekman,et al.  DIFFERENCES Universals and Cultural Differences in the Judgments of Facial Expressions of Emotion , 2004 .

[29]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[30]  Hong Shan,et al.  Quantitative diffusion tensor deterministic and probabilistic fiber tractography in relapsing-remitting multiple sclerosis. , 2011, European journal of radiology.

[31]  Rupert Faltermeier,et al.  Probabilistic vs. deterministic fiber tracking and the influence of different seed regions to delineate cerebellar‐thalamic fibers in deep brain stimulation , 2017, The European journal of neuroscience.

[32]  Albert Gjedde,et al.  Emotional valence modulates activity in the posterior fusiform gyrus and inferior medial prefrontal cortex in social perception , 2003, NeuroImage.

[33]  Kwok-Fai So,et al.  The Dorsal Raphe Nucleus Receives Afferents From Alpha-Like Retinal Ganglion Cells and Intrinsically Photosensitive Retinal Ganglion Cells in the Rat. , 2015, Investigative ophthalmology & visual science.

[34]  A. Grabowska,et al.  The Nencki Affective Picture System (NAPS): Introduction to a novel, standardized, wide-range, high-quality, realistic picture database , 2013, Behavior research methods.

[35]  Daniel Weintraub,et al.  Recognition and Treatment of Depression in Parkinson's Disease , 2003, Journal of geriatric psychiatry and neurology.

[36]  Kotagiri Ramamohanarao,et al.  Mapping connectomes with diffusion MRI: deterministic or probabilistic tractography? , 2018, Magnetic resonance in medicine.

[37]  Daniel C Javitt,et al.  DTI and impulsivity in schizophrenia: a first voxelwise correlational analysis , 2004, Neuroreport.

[38]  G. Huston The Hospital Anxiety and Depression Scale. , 1987, The Journal of rheumatology.

[39]  Pierre Besson,et al.  MRI atlas of the human hypothalamus , 2012, NeuroImage.

[40]  Ralph Adolphs,et al.  Fear, faces, and the human amygdala , 2008, Current Opinion in Neurobiology.

[41]  Jeesun Kim,et al.  Emotional expressions evoke a differential response in the fusiform face area , 2013, Front. Hum. Neurosci..

[42]  Anthony J. Sherbondy,et al.  ConTrack: finding the most likely pathways between brain regions using diffusion tractography. , 2008, Journal of vision.

[43]  Colm G. Connolly,et al.  Fusiform Gyrus Dysfunction is Associated with Perceptual Processing Efficiency to Emotional Faces in Adolescent Depression: A Model-Based Approach , 2016, Front. Psychol..

[44]  T. Joh,et al.  Neuropathology of immunohistochemically identified brainstem neurons in Parkinson's disease , 1990, Annals of neurology.

[45]  Marta I Garrido,et al.  An afferent white matter pathway from the pulvinar to the amygdala facilitates fear recognition , 2019, eLife.

[46]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[47]  Deborah A Yurgelun-Todd,et al.  Sex differences in the relationship between white matter microstructure and impulsivity in adolescents. , 2006, Magnetic resonance imaging.

[48]  H. Ruley,et al.  Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC , 2010, Nature Neuroscience.

[49]  Philip A. Kragel,et al.  Decoding the Nature of Emotion in the Brain , 2016, Trends in Cognitive Sciences.

[50]  D. Matsumoto Ethnic differences in affect intensity, emotion judgments, display rule attitudes, and self-reported emotional expression in an American sample , 1993 .

[51]  Hongtu Zhu,et al.  An affective circumplex model of neural systems subserving valence, arousal, and cognitive overlay during the appraisal of emotional faces , 2008, Neuropsychologia.

[52]  Ajay B. Satpute,et al.  The Brain Basis of Positive and Negative Affect: Evidence from a Meta-Analysis of the Human Neuroimaging Literature. , 2016, Cerebral cortex.

[53]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

[54]  M. Elkind,et al.  Stimulus-induced pathologic laughter due to basilar artery dissection , 2005, Neurology.

[55]  Kwok-Fai So,et al.  Light Deprivation Induces Depression-Like Behavior and Suppresses Neurogenesis in Diurnal Mongolian Gerbil (Meriones unguiculatus) , 2011, Cell transplantation.

[56]  Karl J. Friston,et al.  Ten simple rules for dynamic causal modeling , 2010, NeuroImage.

[57]  B. Wandell,et al.  Children's Reading Performance is Correlated with White Matter Structure Measured by Diffusion Tensor Imaging , 2005, Cortex.

[58]  N. Makris,et al.  Hypothalamic Abnormalities in Schizophrenia: Sex Effects and Genetic Vulnerability , 2007, Biological Psychiatry.

[59]  Sheung-Tak Cheng,et al.  The Development and Validation of an Index of Emotional Disposition and Mood State: The Chinese Affect Scale , 1996 .

[60]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[61]  Peter A. Bos,et al.  The Basolateral Amygdala Is Essential for Rapid Escape: A Human and Rodent Study , 2018, Cell.

[62]  Ken-ichi Tabei,et al.  Inferior Frontal Gyrus Activation Underlies the Perception of Emotions, While Precuneus Activation Underlies the Feeling of Emotions during Music Listening , 2015, Behavioural neurology.

[63]  JD Frederick Adolf Paola MD,et al.  A Long Story Short , 2015, Journal of General Internal Medicine.

[64]  Stephan Hamann,et al.  Affective Neuroscience: Amygdala's Role in Experiencing Fear , 2011, Current Biology.

[65]  B. Roth,et al.  The expanded biology of serotonin. , 2009, Annual review of medicine.

[66]  B. Everitt,et al.  Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex , 2002, Neuroscience & Biobehavioral Reviews.

[67]  A. Leentjens,et al.  The nosological position of apathy in clinical practice , 2008, Journal of Neurology, Neurosurgery, and Psychiatry.

[68]  Josef Parvizi,et al.  Neuroanatomy of pathological laughing and crying: a report of the American Neuropsychiatric Association Committee on Research. , 2009, The Journal of neuropsychiatry and clinical neurosciences.

[69]  Li Zhang,et al.  ON and OFF retinal ganglion cells differentially regulate serotonergic and GABAergic activity in the dorsal raphe nucleus , 2016, Scientific Reports.

[70]  B. Ellenbroek,et al.  Rodent models in neuroscience research: is it a rat race? , 2016, Disease Models & Mechanisms.

[71]  G. Vandewalle,et al.  Brain Responses to Violet, Blue, and Green Monochromatic Light Exposures in Humans: Prominent Role of Blue Light and the Brainstem , 2007, PloS one.

[72]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[73]  B. Parkinson,et al.  Emotion and motivation , 1995 .

[74]  Georg Auburger,et al.  The Brainstem Pathologies of Parkinson's Disease and Dementia with Lewy Bodies , 2015, Brain pathology.

[75]  Mark M. Gergues,et al.  The role of 5-HT receptors in depression , 2017, Molecular Brain.

[76]  K Nobuhara,et al.  Frontal white matter anisotropy and symptom severity of late-life depression: a magnetic resonance diffusion tensor imaging study , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[77]  E. Fox,et al.  Facial Expressions of Emotion: Are Angry Faces Detected More Efficiently? , 2000, Cognition & emotion.

[78]  Anna Grabowska,et al.  Erratum to: Characterization of the Nencki Affective Picture System by discrete emotional categories (NAPS BE) , 2015, Behavior Research Methods.

[79]  Jia-Hong Gao,et al.  A Pontine Region is a Neural Correlate of the Human Affective Processing Network , 2015, EBioMedicine.

[80]  Catherine E. Hagan 20 – Nervous System , 2012 .

[81]  Lisa Feldman Barrett,et al.  Amygdala and fusiform gyrus temporal dynamics: Responses to negative facial expressions , 2008, BMC Neuroscience.

[82]  Tatia M.C. Lee,et al.  Cognitive and Emotional Dysfunction after Central Pontine Myelinolysis , 2003, Behavioural neurology.

[83]  Qian Tao,et al.  A retinoraphe projection regulates serotonergic activity and looming-evoked defensive behaviour , 2017, Nature Communications.

[84]  Kwok-Fai So,et al.  Direct Retino-Raphe Projection Alters Serotonergic Tone and Affective Behavior , 2013, Neuropsychopharmacology.

[85]  Kwok-Fai So,et al.  Y-Like Retinal Ganglion Cells Innervate the Dorsal Raphe Nucleus in the Mongolian Gerbil (Meriones unguiculatus) , 2011, PloS one.

[86]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[87]  Christian Keysers,et al.  Experience Modulates Vicarious Freezing in Rats: A Model for Empathy , 2011, PloS one.

[88]  J. Friedman,et al.  Neuropsychiatric symptoms in Parkinson's disease , 2011, Movement disorders : official journal of the Movement Disorder Society.

[89]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.