From Postsynaptic Potentials to Spikes in the Genesis of Auditory Spatial Receptive Fields

Space-specific neurons in the owl's inferior colliculus respond only to a sound coming from a particular direction, which is equivalent to a specific combination of interaural time difference (ITD) and interaural level difference (ILD). Comparison of subthreshold postsynaptic potentials (PSPs) and spike output for the same neurons showed that receptive fields measured in PSPs were much larger than those measured in spikes in both ITD and ILD dimensions. Space-specific neurons fire more spikes for a particular ITD than for its phase equivalents (ITD ± 1/F, where F is best frequency). This differential response was much less pronounced in PSPs. The two sides of pyramid-shaped ILD curves were more symmetrical in spikes than in PSPs. Furthermore, monaural stimuli that were ineffective in eliciting spikes induced subthreshold PSPs. The main cause of these changes between PSPs and spikes is thresholding. The spiking threshold did not vary with the kind of acoustic stimuli presented. However, the thresholds of sound-induced first spikes were lower than those of later sound-induced and spontaneous spikes. This change in threshold may account for the sharpening of ITD selectivity during the stimulus. Large changes in receptive fields across single neurons are not unique to the owl's space-specific neurons but occur in mammalian visual and somatosensory cortices, suggesting the existence of general principles in the formation of receptive fields in high-order neurons.

[1]  C. Keller,et al.  Commissural connections mediate inhibition for the computation of interaural level difference in the barn owl , 1992, Journal of Comparative Physiology A.

[2]  M Konishi,et al.  Responses of neurons in the auditory pathway of the barn owl to partially correlated binaural signals. , 1995, Journal of neurophysiology.

[3]  V Bringuier,et al.  An intracellular study of space and time representation in primary visual cortical receptive fields , 1996, Journal of Physiology-Paris.

[4]  William A. Catterall,et al.  Neuromodulation of Na+ channels: An unexpected form of cellular platicity , 2001, Nature Reviews Neuroscience.

[5]  M. Konishi,et al.  Binaural characteristics of units in the owl's brainstem auditory pathway: precursors of restricted spatial receptive fields , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  C. Gray,et al.  Cellular Mechanisms Contributing to Response Variability of Cortical Neurons In Vivo , 1999, The Journal of Neuroscience.

[7]  E I Knudsen,et al.  Computational maps in the brain. , 1987, Annual review of neuroscience.

[8]  M. Carandini,et al.  Membrane Potential and Firing Rate in Cat Primary Visual Cortex , 2000, The Journal of Neuroscience.

[9]  C. Gray,et al.  Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[10]  A Moiseff,et al.  Time and intensity cues are processed independently in the auditory system of the owl , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  W. Armstrong,et al.  A biotin-containing compound N-(2-aminoethyl)biotinamide for intracellular labeling and neuronal tracing studies: Comparison with biocytin , 1991, Journal of Neuroscience Methods.

[12]  Masakazu Konishi Centrally synthesized maps of sensory space , 1986, Trends in Neurosciences.

[13]  M. Volgushev,et al.  Comparison of the selectivity of postsynaptic potentials and spike responses in cat visual cortex , 2000, The European journal of neuroscience.

[14]  M. Konishi,et al.  Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  J A Mazer,et al.  How the owl resolves auditory coding ambiguity. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[16]  E I Knudsen,et al.  Center-surround organization of auditory receptive fields in the owl. , 1978, Science.

[17]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[18]  J I Gold,et al.  A Site of Auditory Experience-Dependent Plasticity in the Neural Representation of Auditory Space in the Barn Owl's Inferior Colliculus , 2000, The Journal of Neuroscience.

[19]  M Konishi,et al.  Auditory Spatial Receptive Fields Created by Multiplication , 2001, Science.

[20]  N. Suga,et al.  Specificity of combination-sensitive neurons for processing of complex biosonar signals in auditory cortex of the mustached bat. , 1983, Journal of neurophysiology.

[21]  D. Ferster,et al.  EPSP-IPSP interactions in cat visual cortex studied with in vivo whole- cell patch recording , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  M Konishi,et al.  A neural map of interaural intensity differences in the brain stem of the barn owl , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  M. Konishi,et al.  A circuit for detection of interaural time differences in the brain stem of the barn owl , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  M Konishi,et al.  Cellular mechanisms for resolving phase ambiguity in the owl's inferior colliculus. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Koichi Mori,et al.  Across-frequency nonlinear inhibition by GABA in processing of interaural time difference , 1997, Hearing Research.

[26]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[27]  Masakazu Konishi,et al.  Cochlear and Neural Delays for Coincidence Detection in Owls , 2001, The Journal of Neuroscience.

[28]  E I Knudsen,et al.  A neural map of auditory space in the owl. , 1978, Science.

[29]  Eric I. Knudsen,et al.  Representation of interaural level difference in the VLVp, the first site of binaural comparison in the barn owl's auditory system , 1994, Hearing Research.

[30]  H. Wagner,et al.  Representation of interaural time difference in the central nucleus of the barn owl's inferior colliculus , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Hermann Wagner,et al.  Receptive Fields of Neurons in the Owl's Auditory Brainstem Change Dynamically , 1990, The European journal of neuroscience.

[32]  Ralph Adolphs Processing of Interaural Level Differences in the Auditory Brainstem of the Barn Owl , 1993 .

[33]  R. S. Waters,et al.  In vivo intracellular recording and labeling of neurons in the forepaw barrel subfield (FBS) of rat somatosensory cortex: possible physiological and morphological substrates for reorganization. , 1996, Neuroreport.

[34]  E. Knudsen,et al.  Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  M. Konishi,et al.  Selectivity for interaural time difference in the owl's midbrain , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.