Sensory-evoked high-frequency (γ-band) oscillating potentials in somatosensory cortex of the unanesthetized rat

A 64-channel epipial electrode array was used to investigate high-frequency (gamma-band) oscillations in somatosensory cortex of the unanesthetized and unrestrained rat. Oscillations were evoked by manual stimulation of the vibrissae and mystacial pad. Stimulation of the contralateral vibrissae resulted in a significant increase in gamma-power during 128-ms epochs taken just following stimulus onset compared to the prestimulus baseline. Stimulation of the ipsilateral vibrissae was completely ineffective in evoking gamma-oscillations in any animals. Sensory evoked gamma-oscillations were constrained to primary (SI) and secondary (SII) somatosensory cortex. When averaged to an arbitrary reference of peak times in one of the channels, these oscillations exhibited a systematic temporal organization, propagating from the rostral portion of SI to the barrel field proper, and finally to SII. These spatiotemporal characteristics were probably produced by intracortical pathways within rodent somatosensory cortex. The rostrocaudal propagation of gamma-oscillations within the barrel field may also reflect whisking patterns observed when the vibrissae are used as a sensory array, suggesting that synchronized gamma-oscillations may play a role in assembling punctate afferent information provided by the vibrissae into a coherent representation of a somatosensory stimulus.

[1]  Daniel S. Barth,et al.  High frequency (gamma-band) oscillating potentials in rat somatosensory and auditory cortex , 1995, Brain Research.

[2]  William Sutherling,et al.  Current source-density and neuromagnetic analysis of the direct cortical response in rat cortex , 1988, Brain Research.

[3]  K. Reinikainen,et al.  Selective attention enhances the auditory 40-Hz transient response in humans , 1993, Nature.

[4]  H. Groenewegen,et al.  Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat , 1991, Neuroscience.

[5]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[6]  T A Woolsey,et al.  Local intra‐ and interlaminar connections in mouse barrel cortex , 1990, The Journal of comparative neurology.

[7]  R. Llinás,et al.  Coherent 40-Hz oscillation characterizes dream state in humans. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Masterton,et al.  The sensory contribution of a single vibrissa's cortical barrel. , 1986, Journal of neurophysiology.

[9]  J. Olavarria,et al.  Areal and laminar organization of corticocortical projections in the rat somatosensory cortex , 1990, The Journal of comparative neurology.

[10]  T. Woolsey,et al.  Structure of layer IV in the somatosensory neocortex of the rat: Description and comparison with the mouse , 1974, The Journal of comparative neurology.

[11]  J. Prechtl,et al.  Visual motion induces synchronous oscillations in turtle visual cortex. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[12]  E. Fetz,et al.  Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. , 1996, Journal of neurophysiology.

[13]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[14]  D. Barth,et al.  Comparison of evoked potentials and high-frequency (gamma-band) oscillating potentials in rat auditory cortex. , 1995, Journal of neurophysiology.

[15]  D. Simons,et al.  Biometric analyses of vibrissal tactile discrimination in the rat , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[17]  S. Makeig,et al.  A 40-Hz auditory potential recorded from the human scalp. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[18]  H. Killackey,et al.  Patterning of local intracortical projections within the vibrissae representation of rat primary somatosensory cortex , 1995, The Journal of comparative neurology.

[19]  M. Nicolelis,et al.  Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. , 1995, Science.

[20]  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.

[21]  D. Barth,et al.  The effects of subcortical lesions on evoked potentials and spontaneous high frequency (gamma-band) oscillating potentials in rat auditory cortex , 1996, Brain Research.

[22]  T. Woolsey,et al.  The structural organization of layer IV in the somatosensory region (S I) of mouse cerebral cortex , 1970 .

[23]  W. Freeman Spatial properties of an EEG event in the olfactory bulb and cortex. , 1978, Electroencephalography and clinical neurophysiology.

[24]  D. Simons,et al.  Thalamic and corticocortical connections of the second somatic sensory area of the mouse , 1987, The Journal of comparative neurology.

[25]  D. Paré,et al.  Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[26]  W. Jenkins,et al.  Vibrissal roughness discrimination is barrelcortex-dependent , 1992, Behavioural Brain Research.

[27]  D. Barth,et al.  Inter- and intra-hemispheric spatiotemporal organization of spontaneous electrocortical oscillations. , 1996, Journal of neurophysiology.

[28]  J. Donoghue,et al.  Oscillations in local field potentials of the primate motor cortex during voluntary movement. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[29]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[30]  Alexander A. Borbély,et al.  High-frequency components of the rat electrocorticogram are modulated by the vigilance states , 1994, Neuroscience Letters.

[31]  D. Barth,et al.  Thalamic modulation of high-frequency oscillating potentials in auditory cortex , 1996, Nature.

[32]  E. Adrian Olfactory reactions in the brain of the hedgehog , 1942, The Journal of physiology.

[33]  D. Barth,et al.  Topographic analysis of field potentials in rat vibrissa/barrel cortex , 1991, Brain Research.

[34]  G. Macchi,et al.  Different Weights of Subcortico-Cortical Projections upon Primary Sensory Areas: the Thalamic Anterior Intralaminar System , 1993 .

[35]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.