Touch and go: decision-making mechanisms in somatosensation.

A complex sequence of neural events unfolds between sensory receptor activation and motor activity. To understand the underlying decision-making mechanisms linking somatic sensation and action, we ask what components of the neural activity evoked by a stimulus are directly related to psychophysical performance, and how are they related. We find that single-neuron responses in primary and secondary somatosensory cortices account for the observed performance of monkeys in vibrotactile discrimination tasks, and that neuronal and behavioral responses covary in single trials. This sensory activity, which provides input to memory and decision-making mechanisms, is modulated by attention and behavioral context, and microstimulation experiments indicate that it may trigger normal perceptual experiences. Responses recorded in motor areas seem to reflect the output of decision-making operations, which suggests that the ability to make decisions occurs at the sensory-motor interface.

[1]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[2]  V. Mountcastle,et al.  Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture. , 1959, Bulletin of the Johns Hopkins Hospital.

[3]  V. Mountcastle,et al.  THE RELATION OF THALAMIC CELL RESPONSE TO PERIPHERAL STIMULI VARIED OVER AN INTENSIVE CONTINUUM. , 1963, Journal of neurophysiology.

[4]  V. Mountcastle,et al.  NEURAL ACTIVITY IN MECHANORECEPTIVE CUTANEOUS AFFERENTS: STIMULUS-RESPONSE RELATIONS, WEBER FUNCTIONS, AND INFORMATION TRANSMISSION. , 1965, Journal of neurophysiology.

[5]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[6]  V B Mountcastle,et al.  Neural Basis of the Sense of Flutter-Vibration , 1967, Science.

[7]  V. Mountcastle,et al.  The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. , 1968, Journal of neurophysiology.

[8]  J. Hyvärinen,et al.  Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. , 1969, Journal of neurophysiology.

[9]  E. G. Jones,et al.  Commissural and cortico-cortical "columns" in the somatic sensory cortex of primates , 1975, Science.

[10]  H. Künzle Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study inMacaca fascicularis , 1975, Brain Research.

[11]  Mortimer Mishkin,et al.  Analogous neural models for tactual and visual learning , 1979, Neuropsychologia.

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

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

[14]  J. Fuster Prefrontal Cortex , 2018 .

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

[16]  K O Johnson,et al.  Tactile spatial resolution. I. Two-point discrimination, gap detection, grating resolution, and letter recognition. , 1981, Journal of neurophysiology.

[17]  K. O. Johnson,et al.  Tactile spatial resolution. II. Neural representation of Bars, edges, and gratings in monkey primary afferents. , 1981, Journal of neurophysiology.

[18]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[19]  P. Goldman-Rakic,et al.  Delay-related activity of prefrontal neurons in rhesus monkeys performing delayed response , 1982, Brain Research.

[20]  J. Hyvärinen,et al.  Effects of attention on multiunit responses to vibration in the somatosensory regions of the monkey's brain. , 1982, Electroencephalography and clinical neurophysiology.

[21]  J. Ochoa,et al.  Sensations evoked by intraneural microstimulation of single mechanoreceptor units innervating the human hand. , 1983, The Journal of physiology.

[22]  U. Jürgens,et al.  The efferent and afferent connections of the supplementary motor area , 1984, Brain Research.

[23]  M Sur,et al.  Modular distribution of neurons with slowly adapting and rapidly adapting responses in area 3b of somatosensory cortex in monkeys. , 1984, Journal of neurophysiology.

[24]  Elisabeth A. Murray,et al.  Relative contributions of SII and area 5 to tactile discrimination in monkeys , 1984, Behavioural Brain Research.

[25]  T. P. S. Powell,et al.  The ipsilateral cortico-cortical connexions between the cytoarchitectonic subdivisions of the primary somatic sensory cortex in the monkey , 1985, Brain Research Reviews.

[26]  J. Tanji,et al.  Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. I. Responses to instructions determining motor responses to forthcoming signals of different modalities. , 1985, Journal of neurophysiology.

[27]  T. P. S. Powell,et al.  The projection of the primary somatic sensory cortex upon area 5 in the monkey , 1985, Brain Research Reviews.

[28]  J. Tanji,et al.  Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. II. Responses to movement triggering vs. nontriggering sensory signals. , 1985, Journal of neurophysiology.

[29]  G. Leichnetz Afferent and efferent connections of the dorsolateral precentral gyrus (area 4, hand/arm region) in the macaque monkey, with comparisons to area 8 , 1986, The Journal of comparative neurology.

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

[31]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. I. Relations between single cell discharge and direction of movement , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  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.

[34]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[35]  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.

[36]  P. Goldman-Rakic,et al.  Connections of the ventral granular frontal cortex of macaques with perisylvian premotor and somatosensory areas: Anatomical evidence for somatic representation in primate frontal association cortex , 1989, The Journal of comparative neurology.

[37]  K. H. Britten,et al.  Neuronal correlates of a perceptual decision , 1989, Nature.

[38]  E Ahissar,et al.  Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[39]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[40]  G. E. Alexander,et al.  Preparation for movement: neural representations of intended direction in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[41]  G E Alexander,et al.  Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[42]  R. Romo,et al.  Frequency discrimination in the sense of flutter: psychophysical measurements correlated with postcentral events in behaving monkeys , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  G. Orban,et al.  How well do response changes of striate neurons signal differences in orientation: a study in the discriminating monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  D. Burke,et al.  Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. , 1990, The Journal of physiology.

[45]  C. Connor,et al.  Tactile roughness: neural codes that account for psychophysical magnitude estimates , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  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.

[47]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[48]  G L Shulman,et al.  Selective attention in vibrotactile tasks: Detecting the presence and absence of amplitude change , 1991, Perception & psychophysics.

[49]  M Mishkin,et al.  Serial and parallel processing of tactual information in somatosensory cortex of rhesus monkeys. , 1992, Journal of neurophysiology.

[50]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[51]  G. Recanzone,et al.  Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. , 1992, Journal of neurophysiology.

[52]  W. Newsome,et al.  Microstimulation in visual area MT: effects on direction discrimination performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  V B Mountcastle,et al.  Selective output-discriminative signals in the motor cortex of waking monkeys. , 1992, Cerebral cortex.

[54]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  T. Yoshioka,et al.  Neural mechanisms of tactual form and texture perception. , 1992, Annual review of neuroscience.

[56]  J. Phillips,et al.  Responses of human mechanoreceptive afferents to embossed dot arrays scanned across fingerpad skin , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  K. Johnson,et al.  Neural coding of tactile texture: comparison of spatial and temporal mechanisms for roughness perception , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  J Tanji,et al.  Input organization of distal and proximal forelimb areas in the monkey primary motor cortex: A retrograde double labeling study , 1993, The Journal of comparative neurology.

[59]  R. Romo,et al.  Representation of tactile signals in primate supplementary motor area. , 1993, Journal of neurophysiology.

[60]  H Burton,et al.  Neuronal activity in the second somatosensory cortex of monkeys (Macaca mulatta) during active touch of gratings. , 1993, Journal of neurophysiology.

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

[62]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[63]  Apostolos P. Georgopoulos,et al.  New concepts in generation of movement , 1994, Neuron.

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

[65]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[66]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[67]  L Krubitzer,et al.  A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[69]  J. Price,et al.  Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys , 1995, The Journal of comparative neurology.

[70]  R. Romo,et al.  Representation of moving tactile stimuli in the somatic sensory cortex of awake monkeys. , 1995, Journal of neurophysiology.

[71]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[72]  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.

[73]  R. Romo,et al.  Neuronal activity of primate putamen during categorical perception of somaesthetic stimuli , 1995, Neuroreport.

[74]  R. Romo,et al.  Categorization of somaesthetic stimuli: sensorimotor performance and neuronal activity in primary somatic sensory cortex of awake monkeys. , 1996, Neuroreport.

[75]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[76]  J. Fuster,et al.  Mnemonic neuronal activity in somatosensory cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[77]  M N Shadlen,et al.  Motion perception: seeing and deciding. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[78]  Steven S. Hsiao,et al.  Linearity as the basic law of psychophysics: Evidence from studies of the neural mechanisms of roughness magnitude estimation , 1996 .

[79]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque MT , 1996, Visual Neuroscience.

[80]  Emilio Salinas,et al.  Discrimination in the Sense of Flutter: New Psychophysical Measurements in Monkeys , 1997, The Journal of Neuroscience.

[81]  R. Romo,et al.  Categorical perception of somesthetic stimuli: psychophysical measurements correlated with neuronal events in primate medial premotor cortex. , 1997, Cerebral cortex.

[82]  R. Romo,et al.  Functional properties of primate putamen neurons during the categorization of tactile stimuli. , 1997, Journal of neurophysiology.

[83]  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.

[84]  S Kornblum,et al.  Dynamics of Single Neuron Activity in Monkey Primary Motor Cortex Related to Sensorimotor Transformation , 1997, The Journal of Neuroscience.

[85]  D. V. van Essen,et al.  Spatial Attention Effects in Macaque Area V4 , 1997, The Journal of Neuroscience.

[86]  Kenneth O. Johnson,et al.  Neural Coding Mechanisms in Tactile Pattern Recognition: The Relative Contributions of Slowly and Rapidly Adapting Mechanoreceptors to Perceived Roughness , 1997, The Journal of Neuroscience.

[87]  W. Jiang,et al.  Neuronal encoding of texture changes in the primary and the secondary somatosensory cortical areas of monkeys during passive texture discrimination. , 1997, Journal of neurophysiology.

[88]  G. E. Alexander,et al.  Neural correlates of a spatial sensory-to-motor transformation in primary motor cortex. , 1997, Journal of neurophysiology.

[89]  Emilio Salinas,et al.  Role of primary somatic sensory cortex in the categorization of tactile stimuli: effects of lesions , 1997, Experimental Brain Research.

[90]  K. H. Britten,et al.  Electrical microstimulation of cortical area MST biases heading perception in monkeys , 1998, Nature Neuroscience.

[91]  M. Shadlen,et al.  Exploring the Neurophysiology of Decisions , 1998, Neuron.

[92]  E. Seidemann,et al.  Temporal gating of neural signals during performance of a visual discrimination task , 1998, Nature.

[93]  Ehud Ahissar,et al.  Temporal-Code to Rate-Code Conversion by Neuronal Phase-Locked Loops , 1998, Neural Computation.

[94]  Gregory D Horwitz,et al.  Neurophysiology: Sensing and categorizing , 1998, Current Biology.

[95]  E Salinas,et al.  Conversion of Sensory Signals into Motor Commands in Primary Motor Cortex , 1998, The Journal of Neuroscience.

[96]  J. DiCarlo,et al.  Structure of Receptive Fields in Area 3b of Primary Somatosensory Cortex in the Alert Monkey , 1998, The Journal of Neuroscience.

[97]  Ian R. Wickersham,et al.  Neurophysiology: Electrically evoking sensory experience , 1998, Current Biology.

[98]  J. Tanji,et al.  Task-dependent selectivity of movement-related neuronal activity in the primate prefrontal cortex. , 1998, Journal of neurophysiology.

[99]  R. Romo,et al.  Somatosensory discrimination based on cortical microstimulation , 1998, Nature.

[100]  Emilio Salinas,et al.  Neuronal representations in a categorization task: sensory to motor transformation , 1998 .

[101]  Hiroshi Shibasaki,et al.  Attention modulates both primary and second somatosensory cortical activities in humans: a magnetoencephalographic study. , 1998, Journal of neurophysiology.

[102]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[103]  Peter Dayan,et al.  The Effect of Correlated Variability on the Accuracy of a Population Code , 1999, Neural Computation.

[104]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[105]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

[106]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

[107]  J. DiCarlo,et al.  Velocity Invariance of Receptive Field Structure in Somatosensory Cortical Area 3b of the Alert Monkey , 1999, The Journal of Neuroscience.

[108]  '. B.Vallbo Properties of cutaneous mechanoreceptors in the human hand-related to touch sensation , 1999 .

[109]  Carrie J. McAdams,et al.  Effects of Attention on the Reliability of Individual Neurons in Monkey Visual Cortex , 1999, Neuron.

[110]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

[111]  J. Schall,et al.  Neural selection and control of visually guided eye movements. , 1999, Annual review of neuroscience.

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

[113]  J. DiCarlo,et al.  Spatial and Temporal Structure of Receptive Fields in Primate Somatosensory Area 3b: Effects of Stimulus Scanning Direction and Orientation , 2000, The Journal of Neuroscience.

[114]  T. Sejnowski,et al.  Impact of Correlated Synaptic Input on Output Firing Rate and Variability in Simple Neuronal Models , 2000, The Journal of Neuroscience.

[115]  E. Niebur,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2022 .

[116]  R. Romo,et al.  Sensing without Touching Psychophysical Performance Based on Cortical Microstimulation , 2000, Neuron.

[117]  A. Zador,et al.  Neural representation and the cortical code. , 2000, Annual review of neuroscience.

[118]  J. Gold,et al.  Representation of a perceptual decision in developing oculomotor commands , 2000, Nature.

[119]  R. Romo,et al.  Neuronal correlates of sensory discrimination in the somatosensory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[120]  R. Romo,et al.  Periodicity and Firing Rate As Candidate Neural Codes for the Frequency of Vibrotactile Stimuli , 2000, The Journal of Neuroscience.

[121]  J. Collinge Their Causes and Molecular Basis , 2001 .

[122]  J. Takahashi,et al.  Stopping time: the genetics of fly and mouse circadian clocks. , 2001, Annual review of neuroscience.

[123]  P. Best,et al.  Spatial processing in the brain: the activity of hippocampal place cells. , 2001, Annual review of neuroscience.

[124]  M. Sofroniew,et al.  Nerve growth factor signaling, neuroprotection, and neural repair. , 2001, Annual review of neuroscience.

[125]  D. Julius,et al.  The vanilloid receptor: a molecular gateway to the pain pathway. , 2001, Annual review of neuroscience.