Model calculations of steady state responses to binaural stimuli in the dorsal nucleus of the lateral lemniscus

Several studies have been performed in which both the time-dependent and steady state output of cells in the dorsal nucleus of the lateral lemniscus (DNLL) have been measured in response to binaural sound stimulation. In this paper, a mathematical and computational model for the steady state output of DNLL cells is formulated. The model includes ascending connections from both lateral and medial superior olives (LSO and MSO) as well connections from interneurons in the DNLL and connections from the contralateral DNLL through the commissure of Probst. Our intent is to understand how the steady state behavior arises from the cell properties in and connectional patterns from lower brainstem nuclei. In particular, we examine the connectional hypotheses put forward by Markovitz and Pollak (1994) to explain the observed behavior of EI, EI/F, EE/I and EE/FI cells. Using these connections (with minor modifications) and cells with simple input-output relations, we are able to account for the steady state behavior of these cell types. We are able to explain interesting features of the data not commented on before, for example, the initial dip in spike output for EE cells at low ipsilateral sound levels. The presence of an inhibitory interneuron in the DNLL is essential for facilitation. In addition, we examine the effects of the MSO and the commissure of Probst on DNLL output. Furthermore, we propose a simple mechanism by which the cells of the DNLL and LSO could create a topographic place map in the inferior colliculus.

[1]  R. M. Burger,et al.  Analysis of the role of inhibition in shaping responses to sinusoidally amplitude-modulated signals in the inferior colliculus. , 1998, Journal of neurophysiology.

[2]  D. Irvine The Auditory Brainstem , 1986, Progress in Sensory Physiology.

[3]  G D Pollak,et al.  The roles of GABAergic and glycinergic inhibition on binaural processing in the dorsal nucleus of the lateral lemniscus of the mustache bat. , 1994, Journal of neurophysiology.

[4]  Ian M. Winter,et al.  Basilar membrane nonlinearity determines auditory nerve rate-intensity functions and cochlear dynamic range , 1990, Hearing Research.

[5]  J. Kelly,et al.  In vitro brain slice studies of the rat's dorsal nucleus of the lateral lemniscus. III. synaptic pharmacology. , 1996, Journal of neurophysiology.

[6]  M. Reed,et al.  A model for the computation and encoding of azimuthal information by the lateral superior olive. , 1990, The Journal of the Acoustical Society of America.

[7]  Catherine E. Carr,et al.  Processing of Temporal Information in the Brain , 1993 .

[8]  M. Ito,et al.  Sound localization after transection of the commissure of Probst in the albino rat. , 1996, Journal of neurophysiology.

[9]  G D Pollak,et al.  Roles of GABAergic inhibition for the binaural processing of multiple sound sources in the inferior colliculus. , 1997, The Annals of otology, rhinology & laryngology. Supplement.

[10]  J. Kelly Contribution of the Dorsal Nucleus of the Lateral Lemniscus to Binaural Processing in the Auditory Brainstem , 1997 .

[11]  E Covey,et al.  Response properties of single units in the dorsal nucleus of the lateral lemniscus and paralemniscal zone of an echolocating bat. , 1993, Journal of neurophysiology.

[12]  G. Pollak,et al.  Determinants of horizontal sound location selectivity of binaurally excited neurons in an isofrequency region of the mustache bat inferior colliculus. , 1990, Journal of neurophysiology.

[13]  Josef Syka,et al.  Acoustical Signal Processing in the Central Auditory System , 1997, Springer US.

[14]  J. Kelly,et al.  Sound localization after kainic acid lesions of the dorsal nucleus of the lateral lemniscus in the albino rat. , 1996, Behavioral neuroscience.

[15]  Simulation of ILD sensitive neurons in the inferior colliculus of the barn owl , 1998, Hearing Research.

[16]  John F. Brugge,et al.  An Overview of Central Auditory Processing , 1992 .

[17]  G D Pollak,et al.  Azimuthal receptive fields are shaped by GABAergic inhibition in the inferior colliculus of the mustache bat. , 1994, Journal of neurophysiology.

[18]  R. Fay,et al.  The Mammalian auditory pathway : neurophysiology , 1992 .

[19]  R. Fay,et al.  Hearing by Bats , 1995, Springer Handbook of Auditory Research.

[20]  J. Kelly,et al.  Monaural and binaural response properties of single neurons in the rat's dorsal nucleus of the lateral lemniscus , 1998, Hearing Research.

[21]  D. Anderson,et al.  Tonotopic organization and discharge characteristics of single neurons in nuclei of the lateral lemniscus of the cat. , 1970, Journal of neurophysiology.

[22]  Laurel H. Carney,et al.  Spatiotemporal encoding of sound level: Models for normal encoding and recruitment of loudness , 1994, Hearing Research.

[23]  J. Kelly,et al.  Kainic acid lesions of the dorsal nucleus of the lateral lemniscus: effects on binaural evoked responses in rat auditory cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Lichuan Yang,et al.  Features of ipsilaterally evoked inhibition in the dorsal nucleus of the lateral lemniscus , 1998, Hearing Research.

[25]  J. H. Casseday,et al.  The Lower Brainstem Auditory Pathways , 1995 .

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

[27]  G. Pollak,et al.  The Inferior Colliculus , 1995 .

[28]  Masakazu Konishi,et al.  Deciphering the Brain's Codes , 1999, Neural Computation.

[29]  J J Blum,et al.  Further studies of a model for azimuthal encoding: lateral superior olive neuron response curves and developmental processes. , 1991, The Journal of the Acoustical Society of America.

[30]  M. Sachs,et al.  Encoding of steady-state vowels in the auditory nerve: representation in terms of discharge rate. , 1979, The Journal of the Acoustical Society of America.

[31]  D. Anderson,et al.  Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal stimulation. , 1970, Journal of neurophysiology.

[32]  J. Kelly,et al.  Kainic acid lesions of the superior olivary complex: effects on sound localization by the albino rat. , 1998, Behavioral neuroscience.

[33]  L. Yang,et al.  GABA and glycine have different effects on monaural response properties in the dorsal nucleus of the lateral lemniscus of the mustache bat. , 1994, Journal of neurophysiology.

[34]  G. Pollak,et al.  Binaural processing in the dorsal nucleus of the lateral lemniscus , 1994, Hearing Research.

[35]  J. Kelly,et al.  Two sources of inhibition affecting binaural evoked responses in the rat's inferior colliculus : the dorsal nucleus of the lateral lemniscus and the superior olivary complex , 1997, Hearing Research.

[36]  J. Kelly,et al.  Effects of superior olivary comples lesions on binaural responses in rat inferior colliculus , 1992, Brain Research.

[37]  G. Pollak,et al.  The dorsal nucleus of the lateral lemniscus in the mustache bat: Monaural properties , 1993, Hearing Research.

[38]  L. Li,et al.  Inhibitory influence of the dorsal nucleus of the lateral lemniscus on binaural responses in the rat's inferior colliculus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  Nicholas J. Strausfeld,et al.  Neurobiology of Sensory Systems , 1989, Springer US.

[40]  C. Henkel Axonal morphology in fibrodendritic laminae of the dorsal nucleus of the lateral lemniscus: Afferent projections from the medial superior olivary nucleus , 1997, The Journal of comparative neurology.

[41]  G. Pollak The Functional Organization of the Auditory Brainstem in the Mustache Bat and Mechanisms for Sound Localization , 1989 .

[42]  L. Yang,et al.  Differential response properties to amplitude modulated signals in the dorsal nucleus of the lateral lemniscus of the mustache bat and the roles of GABAergic inhibition. , 1997, Journal of neurophysiology.

[43]  J. Kelly,et al.  Contribution of the Dorsal Nucleus of the Lateral Lemniscus to Binaural Responses in the Inferior Colliculus of the Rat: Interaural Time Delays , 1996, The Journal of Neuroscience.

[44]  G. Pollak,et al.  Afferent connections to the dorsal nucleus of the lateral lemniscus of the mustache bat: evidence for two functional subdivisions , 1996, The Journal of comparative neurology.