Stimulus Frequency Processing in Awake Rat Barrel Cortex

In awake rats, we examined the relationship between neural spiking activity in primary somatic sensory cortex and the frequency of whisker stimulation. Neural responses were recorded extracellularly in barrel cortex while single whiskers were deflected with 0.5–18 air puffs per second (apps), a range that includes the whisk rates observed when rats explore their environment and discriminate surfaces with their whiskers. Twenty-nine neurons in layers III and IV were isolated in three rats (23 in barrel columns and 6 in septum columns). At ≤9 apps, cortical neurons responded with one to two spikes per stimulus, whereas at >9 apps, the response efficacy was reduced to only 0.2–0.4 spikes per stimulus. Several mechanisms are discussed that could account for the decrement in responsiveness. Despite this adaptation, neural spike rates increased in direct proportion with stimulus frequency when cast on logarithmic scales. At >9 apps, however, this relationship deteriorated in barrel columns in which the response approximately halved. In contrast, septum column cells continued to increase their spike rates linearly up to 18 apps, although they responded at lower magnitude than the barrel column cells. Our findings suggest that septum column neurons are potential candidates to encode stimulus frequency using spike rate across the entire frequency range relevant to rats' whisking behavior.

[1]  David Kleinfeld,et al.  Active sensation: insights from the rodent vibrissa sensorimotor system , 2006, Current Opinion in Neurobiology.

[2]  M. Nicolelis,et al.  Role of cortical feedback in the receptive field structure and nonlinear response properties of somatosensory thalamic neurons , 2001, Experimental Brain Research.

[3]  Greg C. Champney,et al.  Rate code and temporal code for frequency of whisker stimulation in rat primary and secondary somatic sensory cortex , 2006, Experimental Brain Research.

[4]  J. M. Gibson,et al.  Quantitative studies of stimulus coding in first-order vibrissa afferents of rats. 2. Adaptation and coding of stimulus parameters. , 1983, Somatosensory research.

[5]  B. Connors,et al.  Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  K. Gottschaldt,et al.  Merkel cell receptors: structure and transducer function. , 1981, Science.

[7]  R. Romo,et al.  Neural codes for perceptual discrimination in primary somatosensory cortex , 2005, Nature Neuroscience.

[8]  M. Wong-Riley,et al.  Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[9]  D. Simons Response properties of vibrissa units in rat SI somatosensory neocortex. , 1978, Journal of neurophysiology.

[10]  S Vajda,et al.  Flexible docking of peptides to class I major-histocompatibility-complex receptors. , 1995, Genetic analysis : biomolecular engineering.

[11]  M. Armstrong‐James,et al.  Spatiotemporal convergence and divergence in the rat S1 “Barrel” cortex , 1987, The Journal of comparative neurology.

[12]  S. Hestrin,et al.  Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex , 1998, Nature Neuroscience.

[13]  E. Ahissar,et al.  Parallel Thalamic Pathways for Whisking and Touch Signals in the Rat , 2006, PLoS biology.

[14]  F. Ebner,et al.  Direct inhibition evoked by whisker stimulation in somatic sensory (SI) barrel field cortex of the awake rat. , 2000, Journal of neurophysiology.

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

[16]  Martin Deschênes,et al.  The vibrissal system as a model of thalamic operations. , 2005, Progress in brain research.

[17]  Rune W. Berg,et al.  Activation of nucleus basalis facilitates cortical control of a brain stem motor program. , 2005, Journal of neurophysiology.

[18]  K M Gothard,et al.  Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  E. Guic-Robles,et al.  Rats can learn a roughness discrimination using only their vibrissal system , 1989, Behavioural Brain Research.

[20]  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.

[21]  Anders Dale,et al.  Band-pass response properties of rat SI neurons. , 2003, Journal of neurophysiology.

[22]  S. B. Vincent The function of the vibrissae in the behavior of the white rat , 1912 .

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

[24]  C. Moore Frequency-dependent processing in the vibrissa sensory system. , 2004, Journal of neurophysiology.

[25]  A. Keller,et al.  State-dependent gating of sensory inputs by zona incerta. , 2006, Journal of neurophysiology.

[26]  D. Kleinfeld,et al.  Frisking the Whiskers Patterned Sensory Input in the Rat Vibrissa System , 2004, Neuron.

[27]  F. Ebner,et al.  Barrels and septa: Separate circuits in rat barrel field cortex , 1999, The Journal of comparative neurology.

[28]  M. Castro-Alamancos,et al.  Absence of Rapid Sensory Adaptation in Neocortex during Information Processing States , 2004, Neuron.

[29]  H. Swadlow,et al.  The influence of single VB thalamocortical impulses on barrel columns of rabbit somatosensory cortex. , 2000, Journal of neurophysiology.

[30]  D J Simons,et al.  Thalamic relay of afferent responses to 1- to 12-Hz whisker stimulation in the rat. , 1998, Journal of neurophysiology.

[31]  S. Nelson,et al.  Short-Term Depression at Thalamocortical Synapses Contributes to Rapid Adaptation of Cortical Sensory Responses In Vivo , 2002, Neuron.

[32]  Matteo Carandini,et al.  Somatosensory Integration Controlled by Dynamic Thalamocortical Feed-Forward Inhibition , 2005, Neuron.

[33]  M. Ito Processing of vibrissa sensory information within the rat neocortex. , 1985, Journal of neurophysiology.

[34]  M. Diamond,et al.  Neuronal Encoding of Texture in the Whisker Sensory Pathway , 2005, PLoS biology.

[35]  F. Ebner,et al.  Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus , 1992, The Journal of comparative neurology.

[36]  E Ahissar,et al.  Temporal frequency of whisker movement. II. Laminar organization of cortical representations. , 2001, Journal of neurophysiology.

[37]  A. B. Bonds,et al.  Differential contributions of magnocellular and parvocellular pathways to the contrast response of neurons in bush baby primary visual cortex (V1) , 2000, Visual Neuroscience.

[38]  Erika E. Fanselow,et al.  Behavioral Modulation of Tactile Responses in the Rat Somatosensory System , 1999, The Journal of Neuroscience.

[39]  F. Ebner,et al.  Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: Dependence on the barrel field cortex , 1992, The Journal of comparative neurology.

[40]  J. A. Varela,et al.  Differential Depression at Excitatory and Inhibitory Synapses in Visual Cortex , 1999, The Journal of Neuroscience.

[41]  M. Laubach,et al.  Layer-Specific Somatosensory Cortical Activation During Active Tactile Discrimination , 2004, Science.

[42]  D J Simons,et al.  Cortical columnar processing in the rat whisker-to-barrel system. , 1999, Journal of neurophysiology.

[43]  M. Glickstein,et al.  Whiskers, barrels, and cortical efferent pathways in gap crossing by rats. , 2000, Journal of neurophysiology.

[44]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[45]  D. Contreras,et al.  Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation , 2006, The Journal of Neuroscience.

[46]  D. Simons Temporal and spatial integration in the rat SI vibrissa cortex. , 1985, Journal of neurophysiology.

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

[48]  M. Deschenes,et al.  The Relay of High-Frequency Sensory Signals in the Whisker-to-Barreloid Pathway , 2003, The Journal of Neuroscience.

[49]  Lauren M Jones,et al.  Whisker primary afferents encode temporal frequency of moving gratings , 2006, Somatosensory & motor research.

[50]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[51]  B. Connors,et al.  Efficacy of Thalamocortical and Intracortical Synaptic Connections Quanta, Innervation, and Reliability , 1999, Neuron.

[52]  Michael J Higley,et al.  Integration of synaptic responses to neighboring whiskers in rat barrel cortex in vivo. , 2005, Journal of neurophysiology.

[53]  R. Lin,et al.  Thalamic afferents of the rat barrel cortex: a light- and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. , 1993, Somatosensory & motor research.

[54]  Kevin Fox,et al.  The Origin of Cortical Surround Receptive Fields Studied in the Barrel Cortex , 2003, The Journal of Neuroscience.

[55]  K. Nakamura,et al.  Lateral hypothalamus neuron involvement in integration of natural and artificial rewards and cue signals. , 1986, Journal of neurophysiology.

[56]  M. Armstrong‐James,et al.  Flow of excitation within rat barrel cortex on striking a single vibrissa. , 1992, Journal of neurophysiology.

[57]  M. A. Neimark,et al.  Neural Correlates of Vibrissa Resonance Band-Pass and Somatotopic Representation of High-Frequency Stimuli , 2004, Neuron.

[58]  D. Kleinfeld,et al.  Adaptive Filtering of Vibrissa Input in Motor Cortex of Rat , 2002, Neuron.

[59]  H. Zeigler,et al.  Conditioned whisking in the rat. , 1996, Somatosensory & motor research.

[60]  M. Brecht,et al.  Functional architecture of the mystacial vibrissae , 1997, Behavioural Brain Research.

[61]  D Kleinfeld,et al.  Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. , 1997, Journal of neurophysiology.

[62]  A. Agmon,et al.  Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex , 2001, The Journal of Neuroscience.

[63]  W. Welker Analysis of Sniffing of the Albino Rat 1) , 1964 .

[64]  David Kleinfeld,et al.  Developmental regulation of active and passive membrane properties in rat vibrissa motoneurones , 2004, The Journal of physiology.

[65]  E Ahissar,et al.  Temporal frequency of whisker movement. I. Representations in brain stem and thalamus. , 2001, Journal of neurophysiology.

[66]  D. Contreras,et al.  Voltage-Sensitive Dye Imaging of Neocortical Spatiotemporal Dynamics to Afferent Activation Frequency , 2001, The Journal of Neuroscience.

[67]  Rune W. Berg,et al.  Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. , 2003, Journal of neurophysiology.

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

[69]  M. A. Friedman,et al.  Thalamo‐cortical processing of vibrissal information in the rat. I. Intracortical origins of surround but not centre‐receptive fields of layer IV neurones in the rat S1 barrel field cortex , 1991, The Journal of comparative neurology.

[70]  D. Simons,et al.  Task- and subject-related differences in sensorimotor behavior during active touch. , 1995, Somatosensory & motor research.

[71]  D J Simons,et al.  Adaptation in thalamic barreloid and cortical barrel neurons to periodic whisker deflections varying in frequency and velocity. , 2004, Journal of neurophysiology.

[72]  H. Philip Zeigler,et al.  Whisker Deafferentation and Rodent Whisking Patterns: Behavioral Evidence for a Central Pattern Generator , 2001, The Journal of Neuroscience.

[73]  Gavin W. Jones,et al.  Is demographic uniformity inevitable? , 1993, Journal of the Australian Population Association.

[74]  N. Wittenburg,et al.  Transformation from temporal to rate coding in a somatosensory thalamocortical pathway , 2022 .

[75]  Ford F. Ebner,et al.  Cortical Modulation of Spatial and Angular Tuning Maps in the Rat Thalamus , 2007, The Journal of Neuroscience.

[76]  T. Woolsey,et al.  The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. , 1970, Brain research.