Fine-scale organization of SI (area 3b) in the squirrel monkey revealed with intrinsic optical imaging.

Optical imaging of intrinsic cortical activity was used to study the somatotopic map and the representation of pressure, flutter, and vibration in area 3b of the squirrel monkey (Saimiri sciureus) cortex under pentothal or isoflurane anesthesia. The representation of the fingerpads in primary somatosensory cortex was investigated by stimulating the glabrous skin of distal fingerpads (D1-D5) with Teflon probes (3-mm diam) attached through an armature to force feedback-controlled torque motors. Under pentothal anesthesia, intrinsic signal maps in area 3b obtained in response to stimulation (trapezoidal indentation) of individual fingerpads showed focal activations. These activations (ranging from 0.5 to 1.0 mm) were discrete and exhibited minimal overlap between adjacent fingerpad representations. Consistent with previously published maps, a somatotopic representation of the fingerpads was observed with an orderly medial to lateral progression from the D5 to D1 fingerpads. Under isoflurane anesthesia, general topography was still maintained, but the representation of fingerpads on adjacent fingers had higher degrees of overlap than with pentothal anesthesia. Multi- and single-unit recordings in the activation zones confirmed the somatotopic maps. To examine preferential inputs from slowly adapting type I (SA) and rapidly adapting type I (RA) and type II (PC) mechanoreceptors, we applied stimuli consisting of sinusoidal indentations that produce sensations of pressure (1 Hz), flutter (30 Hz), and vibration (200 Hz). Under pentothal anesthesia, activation patterns to these different stimuli were focal and coincided on the cortex. Under isoflurane, activation zones from pressure, flutter, and vibratory stimuli differed in size and shape and often contained multiple foci, although overall topography was maintained. Subtraction and vector maps revealed cortical areas (approximate 250-microm diam) that were preferentially activated by the sensations of pressure, flutter, and vibration. Multi- and single-unit recordings aided in the interpretation of the imaging maps. In conclusion, the cortical signals observed with intrinsic signal optical imaging delineated a somatotopic organization of area 3b and revealed different topographical cortical activation patterns for pressure, flutter, and vibratory stimuli. These patterns were dependent on anesthesia type. Possible relationships of these anesthesia effects to somatosensory cortical plasticity are discussed.

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

[2]  V. Mountcastle,et al.  Detection thresholds for stimuli in humans and monkeys: comparison with threshold events in mechanoreceptive afferent nerve fibers innervating the monkey hand. , 1972, Journal of neurophysiology.

[3]  J. Kaas,et al.  Modular segregation of functional cell classes within the postcentral somatosensory cortex of monkeys. , 1981, Science.

[4]  M. Stryker,et al.  Anesthetic state does not affect the map of the hand representation within area 3b somatosensory cortex in owl monkey , 1987, The Journal of comparative neurology.

[5]  B L Whitsel,et al.  Mechanisms underlying somatosensory cortical dynamics: I. In vivo studies. , 1992, Cerebral cortex.

[6]  D. Ts'o,et al.  Functional organization of primate visual cortex revealed by high resolution optical imaging. , 1990, Science.

[7]  David P. Friedman,et al.  Corticocortical connections predict patches of stimulus‐evoked metabolic activity in monkey somatosensory cortex , 1990, The Journal of comparative neurology.

[8]  G. Recanzone,et al.  Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. , 1992, Journal of neurophysiology.

[9]  R. Nicoll,et al.  A physiological role for GABAB receptors in the central nervous system , 1988, Nature.

[10]  W von Seelen,et al.  Optical imaging of rat somatosensory cortex reveals representational overlap as topographic principle , 1995, Neuroreport.

[11]  M. Merzenich,et al.  Single-Cell Correlates of a Representational Boundary in Rat Somatosensory Cortex , 1998, The Journal of Neuroscience.

[12]  D. J. Felleman,et al.  Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys , 1983, Neuroscience.

[13]  R D Frostig,et al.  Varying the degree of single-whisker stimulation differentially affects phases of intrinsic signals in rat barrel cortex. , 1999, Journal of neurophysiology.

[14]  M M Merzenich,et al.  Optical imaging and electrophysiology of rat barrel cortex. I. Responses to small single-vibrissa deflections. , 1998, Cerebral cortex.

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

[16]  B. Antkowiak,et al.  Different actions of general anesthetics on the firing patterns of neocortical neurons mediated by the GABA(A) receptor. , 1999, Anesthesiology.

[17]  J. Kaas,et al.  Large-scale functional reorganization in adult monkey cortex after peripheral nerve injury. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Kaas,et al.  Variability in hand surface representations in areas 3b and 1 in adult owl and squirrel monkeys , 1987, The Journal of comparative neurology.

[19]  G. Blasdel,et al.  Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  A. P. Georgopoulos,et al.  Movement parameters and neural activity in motor cortex and area 5. , 1994, Cerebral cortex.

[21]  G. Ghose,et al.  Form processing modules in primate area V4. , 1997, Journal of neurophysiology.

[22]  M. Merzenich,et al.  Dendritic bias of neurons in rat somatosensory cortex associated with a functional boundary , 1999, The Journal of comparative neurology.

[23]  S. Bolanowski,et al.  Four channels mediate the mechanical aspects of touch. , 1988, The Journal of the Acoustical Society of America.

[24]  M. Sur,et al.  Temporal modulation of spatial borders in rat barrel cortex. , 1998, Journal of neurophysiology.

[25]  D. Ts'o,et al.  Visual topography in primate V2: multiple representation across functional stripes , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  G. Essick,et al.  SI neuron response variability is stimulus tuned and NMDA receptor dependent. , 1999, Journal of neurophysiology.

[27]  R. T. Verrillo.  TEMPORAL SUMMATION IN VIBROTACTILE SENSITIVITY. , 1965, The Journal of the Acoustical Society of America.

[28]  A. Grinvald,et al.  Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during spiral tracing. , 1999, Journal of neurophysiology.

[30]  M. Stryker,et al.  Ocular dominance peaks at pinwheel center singularities of the orientation map in cat visual cortex. , 1997, Journal of neurophysiology.

[31]  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.

[32]  B L Whitsel,et al.  Response of anterior parietal cortex to different modes of same-site skin stimulation. , 1998, Journal of neurophysiology.

[33]  R. Johansson,et al.  Responses of mechanoreceptive afferent units in the glabrous skin of the human hand to sinusoidal skin displacements , 1982, Brain Research.

[34]  A. Grinvald,et al.  Relationships between orientation-preference pinwheels, cytochrome oxidase blobs, and ocular-dominance columns in primate striate cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[35]  R. Bickford,et al.  The classification and significance of electro-encephalographic patterns produced by nitrous oxide-ether anesthesia during surgical operations. , 1950, Proceedings of the staff meetings. Mayo Clinic.

[36]  G. Blasdel,et al.  Orientation selectivity, preference, and continuity in monkey striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  M. Merzenich,et al.  Representation of slowly and rapidly adapting cutaneous mechanoreceptors of the hand in Brodmann's areas 3 and 1 of Macaca mulatta. , 1972, Brain research.

[38]  B. Whitsel,et al.  Metabolic labeling associated with index finger stimulation in monkey SI: Between animal variability , 1985, Brain Research.

[39]  R. Dykes,et al.  Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. , 1984, Journal of neurophysiology.

[40]  C E Schroeder,et al.  Electrophysiological evidence for overlapping dominant and latent inputs to somatosensory cortex in squirrel monkeys. , 1995, Journal of neurophysiology.

[41]  J. Kaas,et al.  The somatotopic organization of area 2 in macaque monkeys , 1985, The Journal of comparative neurology.

[42]  R D Frostig,et al.  Characterization of functional organization within rat barrel cortex using intrinsic signal optical imaging through a thinned skull. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[43]  J. Mayhew,et al.  Cerebral Vasomotion: A 0.1-Hz Oscillation in Reflected Light Imaging of Neural Activity , 1996, NeuroImage.

[44]  H. E. Torebjörk,et al.  Specific sensations evoked by activity in single identified sensory units in man. , 1980 .

[45]  B. Whitsel,et al.  Dose- and time-dependent effects of ketamine on SI neurons with cutaneous receptive fields. , 1982, Journal of neurophysiology.

[46]  Mriganka Sur,et al.  Somatosensory cortex in macaque monkeys: laminar differences in receptive field size in areas 3b and 1 , 1985, Brain Research.

[47]  Mriganka Sur,et al.  Morphology of single intracellularly stained axons terminating in area 3b of macaque monkeys , 1990, The Journal of comparative neurology.

[48]  B. Whitsel,et al.  Anterior parietal cortical topographic organization in macaque monkey: a reevaluation. , 1982, Journal of neurophysiology.

[49]  Mark Tommerdahl,et al.  Optical imaging of intrinsic signals in somatosensory cortex , 2002, Behavioural Brain Research.

[50]  R. Frostig,et al.  Optical imaging of neuronal activity. , 1988, Physiological reviews.

[51]  R. Dykes,et al.  The organization of two cutaneous submodalities in the forearm region of area 3b of cat somatosensory cortex , 1983, The Journal of comparative neurology.

[52]  S. Nelson,et al.  Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. , 1998, Journal of neurophysiology.

[53]  G A Gescheider,et al.  Psychophysical tuning curves in vibrotaction. , 1978, Sensory processes.

[54]  Christopher R. Stambaugh,et al.  Simultaneous encoding of tactile information by three primate cortical areas , 1998, Nature Neuroscience.

[55]  G. Recanzone,et al.  Expansion of the cortical representation of a specific skin field in primary somatosensory cortex by intracortical microstimulation. , 1992, Cerebral cortex.

[56]  G A Gescheider,et al.  Vibrotactile forward masking: psychophysical evidence for a triplex theory of cutaneous mechanoreception. , 1985, The Journal of the Acoustical Society of America.

[57]  W. H. Stanton,et al.  Electroencephalography in anaesthetic practice. , 1965, British journal of anaesthesia.

[58]  V. Mountcastle,et al.  Capacities of humans and monkeys to discriminate vibratory stimuli of different frequency and amplitude: a correlation between neural events and psychological measurements. , 1975, Journal of neurophysiology.

[59]  A W Roe,et al.  Specificity of color connectivity between primate V1 and V2. , 1999, Journal of neurophysiology.

[60]  O. Franzén,et al.  Somesthesis and the Neurobiology of the Somatosensory Cortex , 1996, Advances in Life Sciences.

[61]  Amiram Grinvald,et al.  Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns , 1991, Nature.

[62]  J. Pettigrew,et al.  Spontaneous and stimulus-evoked intrinsic optical signals in primary auditory cortex of the cat. , 2001, Journal of neurophysiology.

[63]  M. Diamond,et al.  Spatial–Temporal Distribution of Whisker-Evoked Activity in Rat Somatosensory Cortex and the Coding of Stimulus Location , 2000, The Journal of Neuroscience.

[64]  B H Pubols,et al.  Relations between stimulus force, skin displacement, and discharge characteristics of slowly adapting type I cutaneous mechanoreceptors in glabrous skin of squirrel monkey hand. , 1986, Somatosensory research.

[65]  P. Dutar,et al.  An iontophoretic study of single somatosensory neurons in rat granular cortex serving the limbs: a laminar analysis of glutamate and acetylcholine effects on receptive-field properties. , 1988, Journal of neurophysiology.

[66]  Chantal Couture,et al.  Mechanisms of action , 1994, Schizophrenia Research.

[67]  J. Kaas,et al.  A histologically visible representation of the fingers and palm in primate area 3b and its immutability following long-term deafferentations. , 1998, Cerebral cortex.

[68]  M. Sur,et al.  Subthreshold facilitation and suppression in primary visual cortex revealed by intrinsic signal imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[69]  R B Tootell,et al.  Topography of cytochrome oxidase activity in owl monkey cortex , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  B. Whitsel,et al.  A combined 2‐deoxyglucose and neurophysiological study of primate somatosensory cortex , 1987, The Journal of comparative neurology.

[71]  B. Rockstroh,et al.  Increased Cortical Representation of the Fingers of the Left Hand in String Players , 1995, Science.

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

[73]  J. Kaas,et al.  Consistent features of the representation of the hand in area 3b of macaque monkeys. , 1987, Somatosensory research.

[74]  Christopher R. Stambaugh,et al.  Encoding of Tactile Stimulus Location by Somatosensory Thalamocortical Ensembles , 2000, The Journal of Neuroscience.

[75]  Douglas G. Kelly,et al.  Local receptive field diversity within cortical neuronal populations , 1996 .

[76]  M. Stryker,et al.  Spatial Frequency Maps in Cat Visual Cortex , 2000, The Journal of Neuroscience.

[77]  J. Kaas,et al.  Representations of the body surface in cortical areas 3b and 1 of squirrel monkeys: Comparisons with other primates , 1982, The Journal of comparative neurology.

[78]  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.

[79]  B. Connors,et al.  Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. , 1999, Journal of neurophysiology.

[80]  E. Todorov.  Direct cortical control of muscle activation in voluntary arm movements: a model , 2000, Nature Neuroscience.

[81]  C. Gilbert,et al.  Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex , 1995, Nature.

[82]  D J Simons,et al.  Laminar differences in bicuculline methiodide's effects on cortical neurons in the rat whisker/barrel system. , 1998, Somatosensory & motor research.

[83]  B. Whitsel,et al.  Response of anterior parietal cortex to cutaneous flutter versus vibration. , 1999, Journal of neurophysiology.

[84]  B L Whitsel,et al.  Mechanisms underlying somatosensory cortical dynamics: II. In vitro studies. , 1992, Cerebral cortex.

[85]  R. Bickford,et al.  Electro-encephalographic patterns produced by thiopental sodium during surgical operations; description and classification. , 1951, British journal of anaesthesia.

[86]  I. Pichlmayr,et al.  The electroencephalogram in anesthesiology : fundamentals, practical applications, examples , 1984 .