Reversible deactivation of higher-order posterior parietal areas. II. Alterations in response properties of neurons in areas 1 and 2.

The role that posterior parietal (PPC) and motor cortices play in modulating neural responses in somatosensory areas 1 and 2 was examined with reversible deactivation by transient cooling. Multiunit recordings from neurons in areas 1 and 2 were collected from six anesthetized adult monkeys (Macaca mulatta) before, during, and after reversible deactivation of areas 5L or 7b or motor cortex (M1/PM), while select locations on the hand and forelimb were stimulated. Response changes were quantified as increases and decreases to stimulus-driven activity relative to baseline and analyzed during three recording epochs: during deactivation ("cool") and at two time points after deactivation ("rewarm 1," "rewarm 2"). Although the type of response change observed was variable, for neurons at the recording sites tested >90% exhibited a significant change in response during cooling of 7b while cooling area 5L or M1/PM produced a change in 75% and 64% of sites, respectively. These results suggest that regions in the PPC, and to a lesser extent motor cortex, shape the response characteristics of neurons in areas 1 and 2 and that this kind of feedback modulation is necessary for normal somatosensory processing. Furthermore, this modulation appears to happen on a minute-by-minute basis and may serve as the substrate for phenomena such as somatosensory attention.

[1]  Richard T Born,et al.  Corticocortical Feedback Contributes to Surround Suppression in V1 of the Alert Primate , 2013, The Journal of Neuroscience.

[2]  Cyrille C. Girardin,et al.  Cooling in cat visual cortex: stability of orientation selectivity despite changes in responsiveness and spike width , 2009, Neuroscience.

[3]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

[4]  Leah Krubitzer,et al.  The organization and connections of anterior and posterior parietal cortex in titi monkeys: do New World monkeys have an area 2? , 2005, Cerebral cortex.

[5]  E. P. Gardner,et al.  A quantitative analysis of responses of direction-sensitive neurons in somatosensory cortex of awake monkeys. , 1980, Journal of neurophysiology.

[6]  D. Blake,et al.  Different Neuroplasticity for Task Targets and Distractors , 2011, PloS one.

[7]  J. Hyvärinen,et al.  I. Functional properties of neurons in lateral part of associative area 7 in awake monkeys , 1979, Experimental Brain Research.

[8]  R. Andersen,et al.  Posterior Parietal Cortex Encodes Autonomously Selected Motor Plans , 2007, Neuron.

[9]  Kenneth O. Johnson,et al.  Spatiotemporal Receptive Fields of Peripheral Afferents and Cortical Area 3b and 1 Neurons in the Primate Somatosensory System , 2006, The Journal of Neuroscience.

[10]  J. Bullier,et al.  Visual activity in area V2 during reversible inactivation of area 17 in the macaque monkey. , 1989, Journal of neurophysiology.

[11]  R. Andersen,et al.  The parietal reach region codes the next planned movement in a sequential reach task. , 2001, Journal of neurophysiology.

[12]  O. Hikosaka,et al.  Converging patterns of finger representation and complex response properties of neurons in area 1 of the first somatosensory cortex of the conscious monkey , 1983, Experimental Brain Research.

[13]  Stephen G. Lomber,et al.  The cryoloop: an adaptable reversible cooling deactivation method for behavioral or electrophysiological assessment of neural function , 1999, Journal of Neuroscience Methods.

[14]  M. Tanaka,et al.  Processing of tactile and kinesthetic signals from bilateral sides of the body in the postcentral gyrus of awake monkeys , 2002, Behavioural Brain Research.

[15]  K. Sasaki,et al.  Compensatory motor function of the somatosensory cortex for the motor cortex temporarily impaired by cooling in the monkey , 2004, Experimental Brain Research.

[16]  Simon B. Eickhoff,et al.  BA3b and BA1 activate in a serial fashion after median nerve stimulation: Direct evidence from combining source analysis of evoked fields and cytoarchitectonic probabilistic maps , 2011, NeuroImage.

[17]  Mikhail A Lebedev,et al.  Simultaneous Top-down Modulation of the Primary Somatosensory Cortex and Thalamic Nuclei during Active Tactile Discrimination , 2013, The Journal of Neuroscience.

[18]  E P Gardner,et al.  Temporal integration of multiple-point stimuli in primary somatosensory cortical receptive fields of alert monkeys. , 1980, Journal of neurophysiology.

[19]  G. E. Alexander,et al.  Effects of cooling prefrontal cortex on cell firing in the nucleus medialis dorsalis. , 1973, Brain research.

[20]  Leah Krubitzer,et al.  Organization of area 3a in macaque monkeys: Contributions to the cortical phenotype , 2004, The Journal of comparative neurology.

[21]  J Hyvärinen,et al.  Regional distribution of functions in parietal association area 7 of the monkey. , 1981, Brain research.

[22]  H. Condé,et al.  Effects of local cooling upon conduction and synaptic transmission. , 1972, Brain research.

[23]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

[24]  G. M. Murray,et al.  Parallel processing in rabbit first (SI) and second (SII) somatosensory cortical areas: effects of reversible inactivation by cooling of SI on responses in SII. , 1992, Journal of neurophysiology.

[25]  J. Kaas,et al.  Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: A correlative anatomical and electrophysiological study , 1986, The Journal of comparative neurology.

[26]  M. Rowe,et al.  Parallel processing of tactile information in cat cerebral cortex: effect of reversible inactivation of SII on SI responses. , 1995, Journal of neurophysiology.

[27]  J Hyvärinen,et al.  Receptive field integration and submodality convergence in the hand area of the post‐central gyrus of the alert monkey. , 1978, The Journal of physiology.

[28]  S S Hsiao,et al.  Spatial pattern representation and transformation in monkey somatosensory cortex. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[29]  D. Ferrington,et al.  Parallel processing of tactile information in the cerebral cortex of the cat: effect of reversible inactivation of SI on responsiveness of SII neurons. , 1992, Journal of neurophysiology.

[30]  Matthias M. Müller,et al.  Sustained Spatial Attention to Vibrotactile Stimulation in the Flutter Range: Relevant Brain Regions and Their Interaction , 2013, PloS one.

[31]  T. Yin,et al.  Subcortical projections of the inferior parietal cortex (area 7) in the stump‐tailed monkey , 1984, The Journal of comparative neurology.

[32]  J. H. Kaas,et al.  Ablations of areas 3a and 3b of monkey somatosensory cortex abolish cutaneous responsivity in area 1 , 1990, Brain Research.

[33]  F. Duffy,et al.  Somatosensory System: Organizational Hierarchy from Single Units in Monkey Area 5 , 1971, Science.

[34]  Johan D. Carlin,et al.  Choosing the Rules: Distinct and Overlapping Frontoparietal Representations of Task Rules for Perceptual Decisions , 2013, The Journal of Neuroscience.

[35]  H Burton,et al.  Tactile-spatial and cross-modal attention effects in the second somatosensory and 7b cortical areas of rhesus monkeys. , 1997, Somatosensory & motor research.

[36]  Dominique L. Pritchett,et al.  Cued Spatial Attention Drives Functionally Relevant Modulation of the Mu Rhythm in Primary Somatosensory Cortex , 2010, The Journal of Neuroscience.

[37]  P. Goldman-Rakic,et al.  Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. , 2000, Journal of neurophysiology.

[38]  Lee E Miller,et al.  Responses of somatosensory area 2 neurons to actively and passively generated limb movements. , 2013, Journal of neurophysiology.

[39]  C. Darian‐Smith,et al.  Comparing thalamocortical and corticothalamic microstructure and spatial reciprocity in the macaque ventral posterolateral nucleus (VPLc) and medial pulvinar , 1999, The Journal of comparative neurology.

[40]  Y. Okada,et al.  The effects of cooling and rewarming on the neuronal activity of pyramidal neurons in guinea pig hippocampal slices , 2001, Brain Research.

[41]  Okihide Hikosaka,et al.  Overlapping representation of fingers in the somatosensory cortex (area 2) of the conscious monkey , 1980, Brain Research.

[42]  Phillip I. Good,et al.  Resampling Methods: A Practical Guide to Data Analysis , 2005 .

[43]  M. Sur,et al.  Representations of the body surface in postcentral parietal cortex of Macaca fascicularis , 1980, The Journal of comparative neurology.

[44]  D. Cheyne,et al.  Cortical dynamics of selective attention to somatosensory events , 2010, NeuroImage.

[45]  O. Hikosaka,et al.  Vertical neuronal arrays in the postcentral gyrus signaling active touch: a receptive field study in the conscious monkey , 2004, Experimental Brain Research.

[46]  Larry E. Roberts,et al.  Functional Organization of Primary Somatosensory Cortex Depends on the Focus of Attention , 2002, NeuroImage.

[47]  Stephen G Lomber,et al.  Reciprocal Modulatory Influences between Tonotopic and Nontonotopic Cortical Fields in the Cat , 2010, The Journal of Neuroscience.

[48]  R. Born,et al.  Integrating motion and depth via parallel pathways , 2008, Nature Neuroscience.

[49]  G. T. Coleman,et al.  Hierarchical equivalence of somatosensory areas I and II for tactile processing in the cerebral cortex of the marmoset monkey. , 2001, Journal of neurophysiology.

[50]  El-Mehdi Meftah,et al.  Effects of a cross-modal manipulation of attention on somatosensory cortical neuronal responses to tactile stimuli in the monkey. , 2002, Journal of neurophysiology.

[51]  G. Luppino,et al.  Cortical connections of the inferior parietal cortical convexity of the macaque monkey. , 2006, Cerebral cortex.

[52]  P A Salin,et al.  Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. , 1992, Journal of neurophysiology.

[53]  Leah Krubitzer,et al.  Lesions in Posterior Parietal Area 5 in Monkeys Result in Rapid Behavioral and Cortical Plasticity , 2010, The Journal of Neuroscience.

[54]  L. Leinonen,et al.  II. Functional properties of cells in anterolateral part of area 7 associative face area of awake monkeys , 1979, Experimental Brain Research.

[55]  G M Murray,et al.  Parallel processing in cerebral cortex of the marmoset monkey: effect of reversible SI inactivation on tactile responses in SII. , 1996, Journal of neurophysiology.

[56]  E. Chudler,et al.  Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanesthetized monkeys. , 1994, Journal of neurophysiology.

[57]  R. Andersen,et al.  Neural Dynamics in Monkey Parietal Reach Region Reflect Context-Specific Sensorimotor Transformations , 2006, The Journal of Neuroscience.

[58]  S. Francis,et al.  Within-Digit Functional Parcellation of Brodmann Areas of the Human Primary Somatosensory Cortex Using Functional Magnetic Resonance Imaging at 7 Tesla , 2012, The Journal of Neuroscience.

[59]  G. Rizzolatti,et al.  Functional Organization of Inferior Parietal Lobule Convexity in the Macaque Monkey: Electrophysiological Characterization of Motor, Sensory and Mirror Responses and Their Correlation with Cytoarchitectonic Areas , 2022 .

[60]  C. E. Chapman,et al.  Discharge properties of neurones in the hand area of primary somatosensory cortex in monkeys in relation to the performance of an active tactile discrimination task , 2004, Experimental Brain Research.

[61]  Carlos R. Ponce,et al.  Contributions of Indirect Pathways to Visual Response Properties in Macaque Middle Temporal Area MT , 2011, The Journal of Neuroscience.

[62]  C. Darian‐Smith,et al.  Ipsilateral cortical projections to areas 3a, 3b, and 4 in the macaque monkey , 1993, The Journal of comparative neurology.

[63]  E P Gardner,et al.  Spatial integration of multiple-point stimuli in primary somatosensory cortical receptive fields of alert monkeys. , 1980, Journal of Neurophysiology.

[64]  Soumya Ghosh,et al.  Neurophysiology of prehension. II. Response diversity in primary somatosensory (S-I) and motor (M-I) cortices. , 2007, Journal of neurophysiology.

[65]  Tingrui Pan,et al.  Reversible deactivation of higher-order posterior parietal areas. I. Alterations of receptive field characteristics in early stages of neocortical processing. , 2014, Journal of neurophysiology.

[66]  Jacqueline Gottlieb,et al.  LIP responses to a popout stimulus are reduced if it is overtly ignored , 2006, Nature Neuroscience.

[67]  J Hyvärinen,et al.  Movement‐sensitive and direction and orientation‐selective cutaneous receptive fields in the hand area of the post‐central gyrus in monkeys. , 1978, The Journal of physiology.

[68]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[69]  B E Stein,et al.  Effects of cooling somatosensory cortex on response properties of tactile cells in the superior colliculus. , 1986, Journal of neurophysiology.

[70]  Wim Vanduffel,et al.  Grasping-Related Functional Magnetic Resonance Imaging Brain Responses in the Macaque Monkey , 2011, The Journal of Neuroscience.

[71]  El-Mehdi Meftah,et al.  Independent controls of attentional influences in primary and secondary somatosensory cortex. , 2005, Journal of neurophysiology.

[72]  J. Kaas,et al.  Thalamocortical connections of parietal somatosensory cortical fields in macaque monkeys are highly divergent and convergent. , 2009, Cerebral cortex.

[73]  H. Burton, R. J. Sinclair,et al.  Tactile-spatial and cross-modal attention effects in the primary somatosensory cortical areas 3b and 1-2 of rhesus monkeys , 2000, Somatosensory & motor research.

[74]  Leah Krubitzer,et al.  Topographic Maps within Brodmann's Area 5 of macaque monkeys. , 2012, Cerebral cortex.

[75]  P A Salin,et al.  Visual activity in areas V3a and V3 during reversible inactivation of area V1 in the macaque monkey. , 1991, Journal of neurophysiology.

[76]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[77]  Iwona Stepniewska,et al.  Cortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in new world monkeys. , 2011, Cerebral cortex.

[78]  H Burton,et al.  Tactile attention tasks enhance activation in somatosensory regions of parietal cortex: a positron emission tomography study. , 1999, Cerebral cortex.

[79]  Andrew R Mitz,et al.  Somatotopy of monkey premotor cortex examined with microstimulation , 1995, Neuroscience Research.

[80]  Mario Fiorani,et al.  Parallel Evolution of Cortical Areas Involved in Skilled Hand Use , 2007, The Journal of Neuroscience.

[81]  M. Sur Receptive fields of neurons in areas 3b and 1 of somatosensory cortex in monkeys , 1980, Brain Research.

[82]  S S Hsiao,et al.  Effects of selective attention on spatial form processing in monkey primary and secondary somatosensory cortex. , 1993, Journal of neurophysiology.

[83]  Jessie Chen,et al.  Neurophysiology of prehension. I. Posterior parietal cortex and object-oriented hand behaviors. , 2007, Journal of neurophysiology.

[84]  Anna W Roe,et al.  Connectivity of somatosensory cortical area 1 forms an anatomical substrate for the emergence of multifinger receptive fields and complex feature selectivity in the squirrel monkey (Saimiri sciureus) , 2014, The Journal of comparative neurology.

[85]  M. Volgushev,et al.  Probability of transmitter release at neocortical synapses at different temperatures. , 2004, Journal of neurophysiology.

[86]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[87]  J. H. Kaas,et al.  A sequential representation of the occiput, arm, forearm and hand across the rostrocaudal dimension of areas 1, 2 and 5 in macaque monkeys , 1985, Brain Research.

[88]  S. Lomber,et al.  Evidence for Hierarchical Processing in Cat Auditory Cortex: Nonreciprocal Influence of Primary Auditory Cortex on the Posterior Auditory Field , 2009, The Journal of Neuroscience.

[89]  C. E. Chapman,et al.  Discharge properties of neurones in the hand area of primary somatosensory cortex in monkeys in relation to the performance of an active tactile discrimination task , 2004, Experimental Brain Research.

[90]  Jeffrey M Yau,et al.  Representation of tactile curvature in macaque somatosensory area 2. , 2013, Journal of neurophysiology.

[91]  Hansjörg Scherberger,et al.  Context-Specific Grasp Movement Representation in the Macaque Anterior Intraparietal Area , 2009, The Journal of Neuroscience.

[92]  J. Craig,et al.  Shape Invariant Coding of Motion Direction in Somatosensory Cortex , 2010, PLoS biology.

[93]  Mara Fabri,et al.  Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: A revised interpretation of the second somatosensory area in macaque monkeys , 1995, The Journal of comparative neurology.

[94]  J. Kaas,et al.  Corticocortical and collateral thalamocortical connections of postcentral somatosensory cortical areas in squirrel monkeys: a double-labeling study with radiolabeled wheatgerm agglutinin and wheatgerm agglutinin conjugated to horseradish peroxidase. , 1985, Somatosensory research.

[95]  O. Hikosaka,et al.  Functional subdivisions representing different finger regions in area 3 of the first somatosensory cortex of the conscious monkey , 1983, Experimental Brain Research.

[96]  Masahiro Sakamoto,et al.  Rostrocaudal gradients in the neuronal receptive field complexity in the finger region of the alert monkey's postcentral gyrus , 2004, Experimental Brain Research.

[97]  S. Jacobson,et al.  The thalamic afferents to the inferior parietal lobule of the rhesus monkey , 1978, The Journal of comparative neurology.

[98]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[99]  V. Mountcastle,et al.  Parietal lobe mechanisms for directed visual attention. , 1977, Journal of neurophysiology.

[100]  Liping Wang,et al.  Behavioral Choice-related Neuronal Activity in Monkey Primary Somatosensory Cortex in a Haptic Delay Task , 2012, Journal of Cognitive Neuroscience.

[101]  J. Kaas,et al.  Connections of area 2 of somatosensory cortex with the anterior pulvinar and subdivisions of the ventroposterior complex in macaque monkeys , 1985, The Journal of comparative neurology.

[102]  D. Blake,et al.  Task-dependent modulation of SI physiological responses to targets and distractors. , 2013, Journal of neurophysiology.

[103]  Dylan F. Cooke,et al.  Fabrication of an inexpensive, implantable cooling device for reversible brain deactivation in animals ranging from rodents to primates. , 2012, Journal of neurophysiology.

[104]  Mario Fiorani,et al.  GABA inactivation of visual area MT modifies the responsiveness and direction selectivity of V2 neurons in Cebus monkeys , 2011, Visual Neuroscience.

[105]  M. Ding,et al.  Attentional modulation of the somatosensory mu rhythm , 2011, Neuroscience.

[106]  O. Hikosaka,et al.  Diversity in receptive field properties of vertical neuronal arrays in the crown of the postcentral gyrus of the conscious monkey , 2004, Experimental Brain Research.

[107]  Natasha M. Maurits,et al.  Functional Magnetic Resonance Imaging Connectivity Analyses Reveal Efference-Copy to Primary Somatosensory Area, BA2 , 2014, PloS one.

[108]  J. Hyvärinen,et al.  Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys. , 1974, Brain : a journal of neurology.

[109]  D. Pandya,et al.  Corticothalamic connections of the posterior parietal cortex in the rhesus monkey , 1985, The Journal of comparative neurology.

[110]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

[111]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[112]  B. Ross,et al.  Attention modulates beta oscillations during prolonged tactile stimulation , 2010, The European journal of neuroscience.

[113]  D. Pandya,et al.  Anatomical investigation of projections from thalamus to posterior parietal cortex in the rhesus monkey: A WGA‐HRP and fluorescent tracer study , 1990, The Journal of comparative neurology.

[114]  Jessie Chen,et al.  Neural representation of hand kinematics during prehension in posterior parietal cortex of the macaque monkey. , 2009, Journal of neurophysiology.

[115]  G. Henry,et al.  The effect of reversible cooling of cat's primary visual cortex on the responses of area 21a neurons. , 1993, The Journal of physiology.

[116]  David P. Friedman,et al.  Physiological evidence for serial processing in somatosensory cortex. , 1987, Science.

[117]  A. Iriki,et al.  Bilateral hand representation in the postcentral somatosensory cortex , 1994, Nature.

[118]  Felix Blankenburg,et al.  Tactile Motion and Pattern Processing Assessed with High-Field fMRI , 2011, PloS one.

[119]  Bogdan Dreher,et al.  The effects of reversible inactivation of postero-temporal visual cortex on neuronal activities in cat's area 17 , 2007, Brain Research.

[120]  J Hyvärinen,et al.  Influence of attentive behavior on neuronal responses to vibration in primary somatosensory cortex of the monkey. , 1980, Journal of neurophysiology.

[121]  H Burton,et al.  Ipsilateral intracortical connections of physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: Projections in the vicinity of the central sulcus , 1995, The Journal of comparative neurology.

[122]  J. Kaas,et al.  Multiple representations of the body within the primary somatosensory cortex of primates. , 1979, Science.

[123]  E P Gardner,et al.  Somatosensory cortical mechanisms of feature detection in tactile and kinesthetic discrimination. , 1988, Canadian journal of physiology and pharmacology.

[124]  Elena Borra,et al.  Architectonic organization of the inferior parietal convexity of the macaque monkey , 2006, The Journal of comparative neurology.

[125]  G. Fishell,et al.  A disinhibitory circuit mediates motor integration in the somatosensory cortex , 2013, Nature Neuroscience.

[126]  Iwona Stepniewska,et al.  Thalamocortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in New World monkeys. , 2010, Cerebral cortex.