The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope

Sensory stimuli often have rich temporal and spatial structure. One class of stimuli that are common to visual and auditory systems and, as we show, the electrosensory system are signals that contain power in a narrow range of temporal (or spatial) frequencies. Characteristic of this class of signals is a slower variation in their amplitude, otherwise known as an envelope. There is evidence suggesting that, in the visual cortex, both narrowband stimuli and their envelopes are coded for in separate and parallel streams. The implementation of this parallel transmission is not well understood at the cellular level. We have identified the cellular basis for the parallel transmission of signal and envelope in the electrosensory system: a two-cell network consisting of an interneuron connected to a pyramidal cell by means of a slow synapse. This circuit could, in principle, be implemented in the auditory or visual cortex by the previously identified biophysics of cortical interneurons.

[1]  N. Viemeister.  Temporal modulation transfer functions based upon modulation thresholds. , 1979, The Journal of the Acoustical Society of America.

[2]  J. Bastian,et al.  Commissural neurons of the electrosensory lateral line lobe of Apteronotus leptorhynchus: morphological and physiological characteristics , 1993, Journal of Comparative Physiology A.

[3]  Israel Nelken,et al.  Responses of auditory-cortex neurons to structural features of natural sounds , 1999, Nature.

[4]  Robert Shapley,et al.  Visual cortex: pushing the envelope , 1998, Nature Neuroscience.

[5]  B. L. Cardozo,et al.  Pitch of the Residue , 1962 .

[6]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[7]  Brent Doiron,et al.  Non-classical receptive field mediates switch in a sensory neuron's frequency tuning , 2003, Nature.

[8]  J. B. Demb,et al.  Cellular Basis for the Response to Second-Order Motion Cues in Y Retinal Ganglion Cells , 2001, Neuron.

[9]  C L Baker,et al.  A processing stream in mammalian visual cortex neurons for non-Fourier responses. , 1993, Science.

[10]  Alexander Borst,et al.  Information theory and neural coding , 1999, Nature Neuroscience.

[11]  C. Koch,et al.  Coding of time-varying electric field amplitude modulations in a wave-type electric fish. , 1996, Journal of neurophysiology.

[12]  Eric S. Fortune,et al.  Electrosensory interference in naturally occurring aggregates of a species of weakly electric fish, Eigenmannia virescens , 2005, Behavioural Brain Research.

[13]  Joseph Bastian,et al.  The physiology and morphology of two types of electrosensory neurons in the weakly electric fishApteronotus leptorhynchus , 1984, Journal of Comparative Physiology A.

[14]  Alan V. Oppenheim,et al.  Discrete-Time Signal Pro-cessing , 1989 .

[15]  L. Maler,et al.  Spike-Frequency Adaptation Separates Transient Communication Signals from Background Oscillations , 2005, The Journal of Neuroscience.

[16]  Hiroki Tanaka,et al.  Neural Basis for Stereopsis from Second-Order Contrast Cues , 2006, The Journal of Neuroscience.

[17]  L. Benardo,et al.  Separate activation of fast and slow inhibitory postsynaptic potentials in rat neocortex in vitro. , 1994, The Journal of physiology.

[18]  Xiaoqin Wang,et al.  Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates. , 2002, Journal of neurophysiology.

[19]  E. M. Burns,et al.  Played-again SAM: Further observations on the pitch of amplitude-modulated noise , 1981 .

[20]  John P. Miller,et al.  Assessing the Performance of Neural Encoding Models in the Presence of Noise , 2000, Journal of Computational Neuroscience.

[21]  L. Maler,et al.  The posterior lateral line lobe of certain gymnotoid fish: Quantitative light microscopy , 1979, The Journal of comparative neurology.

[22]  L. Maler,et al.  The cytology of the posterior lateral line lobe of high‐frequency weakly electric fish (gymnotidae): Dendritic differentiation and synaptic specificity in a simple cortex , 1981, The Journal of comparative neurology.

[23]  L. Maler,et al.  Correlating gamma‐aminobutyric acidergic circuits and sensory function in the electrosensory lateral line lobe of a gymnotiform fish , 1994, The Journal of comparative neurology.

[24]  C. Schreiner,et al.  Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fields , 1988, Hearing Research.

[25]  D. McCormick,et al.  Inhibitory Postsynaptic Potentials Carry Synchronized Frequency Information in Active Cortical Networks , 2005, Neuron.

[26]  S. Rice.  Mathematical analysis of random noise , 1944 .

[27]  G. Tamás,et al.  Identified Sources and Targets of Slow Inhibition in the Neocortex , 2003, Science.

[28]  J. Eggermont.  Representation of spectral and temporal sound features in three cortical fields of the cat. Similarities outweigh differences. , 1998, Journal of neurophysiology.

[29]  R. H. Arnott,et al.  Interaural Time Difference Discrimination Thresholds for Single Neurons in the Inferior Colliculus of Guinea Pigs , 2003, The Journal of Neuroscience.

[30]  Michael J. Hawken,et al.  Macaque VI neurons can signal ‘illusory’ contours , 1993, Nature.

[31]  Maurice J Chacron,et al.  Feedback and Feedforward Control of Frequency Tuning to Naturalistic Stimuli , 2005, The Journal of Neuroscience.

[32]  A. Destexhe,et al.  Dual intracellular recordings and computational models of slow inhibitory postsynaptic potentials in rat neocortical and hippocampal slices , 1999, Neuroscience.

[33]  Isabelle Mareschal,et al.  A cortical locus for the processing of contrast-defined contours , 1998, Nature Neuroscience.

[34]  C L Baker,et al.  Spatial properties of envelope-responsive cells in area 17 and 18 neurons of the cat. , 1996, Journal of neurophysiology.

[35]  L. Maler,et al.  Gap junction protein in weakly electric fish (gymnotide): Immunohistochemical localization with emphasis on structures of the electrosensory system , 1989, The Journal of comparative neurology.

[36]  Joseph Bastian,et al.  Descending control of electroreception. I. Properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  L. Maler,et al.  Plastic and Nonplastic Pyramidal Cells Perform Unique Roles in a Network Capable of Adaptive Redundancy Reduction , 2004, Neuron.

[38]  Dante R Chialvo.  How we hear what is not there: a neural mechanism for the missing fundamental illusion. , 2003, Chaos.

[39]  Brent Doiron,et al.  Oscillatory activity in electrosensory neurons increases with the spatial correlation of the stochastic input stimulus. , 2004, Physical review letters.

[40]  Joseph Bastian,et al.  Morphological correlates of pyramidal cell adaptation rate in the electrosensory lateral line lobe of weakly electric fish , 1991, Journal of Comparative Physiology A.

[41]  Maurice J Chacron,et al.  Receptive Field Organization Determines Pyramidal Cell Stimulus-Encoding Capability and Spatial Stimulus Selectivity , 2002, The Journal of Neuroscience.

[42]  L. Maler,et al.  Inhibition evoked from primary afferents in the electrosensory lateral line lobe of the weakly electric fish (Apteronotus leptorhynchus). , 1998, Journal of neurophysiology.

[43]  Maurice J Chacron,et al.  Electroreceptor neuron dynamics shape information transmission , 2005, Nature Neuroscience.

[44]  D. McAlpine,et al.  Neural sensitivity to interaural envelope delays in the inferior colliculus of the guinea pig. , 2005, Journal of neurophysiology.

[45]  David Whitaker,et al.  Spatial characteristics of the second-order visual pathway revealed by positional adaptation , 1999, Nature Neuroscience.

[46]  A. Burkhalter,et al.  Role of GABAB receptor-mediated inhibition in reciprocal interareal pathways of rat visual cortex. , 1999, Journal of neurophysiology.

[47]  T. Sejnowski,et al.  Submicrosecond pacemaker precision is behaviorally modulated: the gymnotiform electromotor pathway. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  C. Baker.  Central neural mechanisms for detecting second-order motion , 1999, Current Opinion in Neurobiology.