Identification of cell types in brain slices of the inferior colliculus

Different type neurons in the inferior colliculus may have different functions. Recent intracellular studies of the inferior colliculus suggest that intrinsic electrical properties contribute to discharge patterns, but the intrinsic discharge patterns have not been fully characterized in the central nucleus, the main part of the inferior colliculus. Whether different types of neurons are related to different discharge patterns is unclear. We have used intracellular and whole-cell patch clamp-recording techniques in a brain slice preparation to better characterize discharge patterns and cell types in the central nucleus. Several types of discharge pattern were found in the inferior colliculus in response to long pulses of intracellular depolarizations. Rebound and buildup-pauser discharges, together, comprise neurons with a sustained response and are the majority of the neurons in the inferior colliculus. Both of these types of discharge pattern could be adapting or regular. Onset discharges distinguished another group of neurons. Onset neurons can also entrain to higher frequency stimuli than sustained neurons. Discharge patterns are correlated with distinctive current-voltage relationships and with some aspects of dendritic morphology. However, the morphological data demonstrates that the discharge patterns do not correspond simply to disc-shaped (flat) or stellate (less-flat) categories. This is the first extensive analysis of electrophysiological properties of the central nucleus of the inferior colliculus in vitro. We suggest that there may be at least three functional classes of neurons and have implications for signal processing in the inferior colliculus.

[1]  R. Batra,et al.  Coding of Sound Envelopes by Inhibitory Rebound in Neurons of the Superior Olivary Complex in the Unanesthetized Rabbit , 1999, The Journal of Neuroscience.

[2]  T. Wagner Intrinsic properties of identified neurones in the central nucleus of mouse inferior colliculus , 1994, NeuroReport.

[3]  K. A. Davis,et al.  Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps. , 1999, Journal of neurophysiology.

[4]  C. Faingold,et al.  In vitro electrophysiology of neurons in subnuclei of rat inferior colliculus , 1998, Hearing Research.

[5]  M. Sachs,et al.  The representations of the steady-state vowel sound /e/ in the discharge patterns of cat anteroventral cochlear nucleus neurons. , 1990, Journal of neurophysiology.

[6]  I. Forsythe,et al.  Two voltage-dependent K+ conductances with complementary functions in postsynaptic integration at a central auditory synapse , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  S Kuwada,et al.  Monaural and binaural response properties of neurons in the inferior colliculus of the rabbit: effects of sodium pentobarbital. , 1989, Journal of neurophysiology.

[8]  W. Shofner,et al.  Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. , 1988, Journal of neurophysiology.

[9]  G. Aghajanian,et al.  Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices , 1989, Synapse.

[10]  W. S. Rhode,et al.  Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus , 1983, The Journal of comparative neurology.

[11]  P. Smith Anatomy and physiology of multipolar cells in the rat inferior collicular cortex using the in vitro brain slice technique , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  K. A. Fitzpatrick Cellular architecture and topographic organization of the inferior colliculus of the squirrel monkey , 1975, The Journal of comparative neurology.

[13]  Nace L. Golding,et al.  Recordings from slices indicate that octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  V. Meininger,et al.  The inferior colliculus of the mouse. A Nissl and Golgi study , 1986, Neuroscience.

[15]  T. Yin,et al.  Dendritic and axonal morphology of HRP‐injected neurons in the inferior colliculus of the cat , 1991, The Journal of comparative neurology.

[16]  S. Wu,et al.  Physiological properties of neurons in the ventral nucleus of the lateral lemniscus of the rat: intrinsic membrane properties and synaptic responses. , 1999, Journal of neurophysiology.

[17]  PB Manis,et al.  Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  A. Rockel,et al.  The neuronal organization of the inferior colliculus of the adult cat. II. The pericentral nucleus , 1973, The Journal of comparative neurology.

[19]  D. Oliver,et al.  Dorsal cochlear nucleus projections to the inferior colliculus in the cat: A light and electron microscopic study , 1984, The Journal of comparative neurology.

[20]  M N Semple,et al.  Single-unit responses in the inferior colliculus: different consequences of contralateral and ipsilateral auditory stimulation. , 1985, Journal of neurophysiology.

[21]  Wilfrid Rall,et al.  Theoretical significance of dendritic trees for neuronal input-output relations , 1964 .

[22]  D. Oertel,et al.  Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice , 1989, The Journal of comparative neurology.

[23]  P. H. Smith,et al.  Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  T. Blackstad,et al.  The central nucleus of the inferior colliculus in rat: A Golgi and computer reconstruction study of neuronal and laminar structure , 1993, The Journal of comparative neurology.

[25]  D. Oertel,et al.  Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  D. Oliver,et al.  The neuronal architecture of the inferior colliculus in the cat: Defining the functional anatomy of the auditory midbrain , 1984, The Journal of comparative neurology.

[27]  J. Adams Heavy metal intensification of DAB-based HRP reaction product. , 1981, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[28]  S Kuwada,et al.  Intracellular Recordings in Response to Monaural and Binaural Stimulation of Neurons in the Inferior Colliculus of the Cat , 1997, The Journal of Neuroscience.

[29]  J. A. Hirsch,et al.  Intrinsic properties of neurones in the dorsal cochlear nucleus of mice, in vitro. , 1988, The Journal of physiology.

[30]  D. Irvine Physiology of the Auditory Brainstem , 1992 .

[31]  S Kuwada,et al.  A comparison of the interaural time sensitivity of neurons in the inferior colliculus and thalamus of the unanesthetized rabbit , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  D. Oertel Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  D. Oliver Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: Possible substrates for binaural interaction , 1987, The Journal of comparative neurology.

[34]  R. Batra,et al.  A physiological and structural study of neuron types in the cochlear nucleus. I. Intracellular responses to acoustic stimulation and current injection , 1994, The Journal of comparative neurology.

[35]  E. Ostapoff,et al.  A physiological and structural study of neuron types in the cochlear nucleus. II. Neuron types and their structural correlation with response properties , 1994, The Journal of comparative neurology.

[36]  Paul B. Manis,et al.  Transient Potassium Currents Regulate the Discharge Patterns of Dorsal Cochlear Nucleus Pyramidal Cells , 1999, The Journal of Neuroscience.

[37]  P. Torterolo,et al.  In vivo intracellular characteristics of inferior colliculus neurons in guinea pigs , 1997, Brain Research.

[38]  K. A. Davis,et al.  Single-unit responses in the inferior colliculus of decerebrate cats. II. Sensitivity to interaural level differences. , 1999, Journal of neurophysiology.

[39]  D. Oertel,et al.  Use of brain slices in the study of the auditory system: spatial and temporal summation of synaptic inputs in cells in the anteroventral cochlear nucleus of the mouse. , 1985, The Journal of the Acoustical Society of America.

[40]  W. S. Rhode,et al.  Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus , 1983, The Journal of comparative neurology.

[41]  A. Reyes,et al.  Membrane properties underlying the firing of neurons in the avian cochlear nucleus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  A. Rees,et al.  Regularity of firing of neurons in the inferior colliculus. , 1997, Journal of neurophysiology.

[43]  E G Jones,et al.  The neuronal organization of the inferior colliculus of the adult cat. I. The central nucleus , 1973, The Journal of comparative neurology.

[44]  W. Rall Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. , 1967, Journal of neurophysiology.

[45]  S Kuwada,et al.  Binaural interaction in low-frequency neurons in inferior colliculus of the cat. IV. Comparison of monaural and binaural response properties. , 1984, Journal of neurophysiology.

[46]  P. Manis,et al.  Outward currents in isolated ventral cochlear nucleus neurons , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  Philip H Smith,et al.  Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: Evidence for delay lines to the medial superior olive , 1993, The Journal of comparative neurology.

[48]  L. Kaczmarek,et al.  Expression of the mRNAs for the Kv3.1 potassium channel gene in the adult and developing rat brain. , 1992, Journal of neurophysiology.

[49]  D. Oliver,et al.  The central nucleus of the inferior colliculus in the cat , 1984, The Journal of comparative neurology.

[50]  Steven Greenberg,et al.  Physiology of the Cochlear Nuclei , 1992 .

[51]  M S Malmierca,et al.  Contribution of GABA- and glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus. , 1996, Journal of neurophysiology.