Auditory cortex neurons sensitive to correlates of auditory motion: underlying mechanisms

SummaryNeuronal response properties such as phasic vs. tonic, onset vs. offset, monotonicity vs. non-monotonicity, and E/E vs. E/I, can be shown to act synergistically suggesting underlying mechanisms for selectivity to binaural intensity correlates of auditory sound source motion. Both identical (diotic), and oppositely directed dichotic AM ramps were used as stimuli in the lightly anesthetized cat, simulating motion in four canonical directions in 3-dimensional space. Motion in either azimuthal direction evokes selective activity in cells which respond best to the onset of monaural sound in one ear and show a decreased response to binaural stimulation (E/I or I/E). In some cells specificity is increased by “off” components in the non-dominant ear. Although these cells fire only at the onset of stationary sound, they fire throughout oppositely directed AM ramps. Motion toward or away from the head evokes responses from EE cells; strong binaural facilitation increases selectivity for motion in depth. The sharpness of direction of tuning was related to the degree of binaural facilitation in E/E cells. Selectivity for sound moving away from the head is correlated with “off” responses, while “on” responses correlate with preference for motion toward the head. Most units showed a monotonic rate function as AM ramp excursion and rate was increased. One third were selective for slower rates of intensity change and may therefore encode slower rates of stimulus motion, as well as direction of movement. The findings suggest that neural processing of auditory motion involves neural mechanisms distinct from those involved in processing stationary sound location and that these mechanisms arise from interactions between the more traditionally studied response properties of auditory cortex neurons.

[1]  J. C. Middlebrooks,et al.  Functional classes of neurons in primary auditory cortex of the cat distinguished by sensitivity to sound location , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  Russell L. Martin,et al.  Interaural sound pressure level differences associated with sound-source locations in the frontal hemifield of the domestic cat , 1989, Hearing Research.

[3]  G. Pollak,et al.  Determinants of sound location selectivity in bat inferior colliculus: a combined dichotic and free-field stimulation study. , 1985, Journal of neurophysiology.

[4]  D Regan,et al.  A stereo field map with implications for disparity processing. , 1973, Investigative ophthalmology.

[5]  T. Pasternak,et al.  Pattern and motion vision in cats with selective loss of cortical directional selectivity , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Lois Anthony,et al.  Evoked Electrical Activity in the Auditory Nervous System , 1979 .

[7]  J. C. Middlebrooks,et al.  A neural code for auditory space in the cat's superior colliculus , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  M. Cynader,et al.  Neurones in cat parastriate cortex sensitive to the direction of motion in three‐dimensional space , 1978, The Journal of physiology.

[9]  M. Cynader,et al.  Neurons in cat primary auditory cortex sensitive to correlates of auditory motion in three-dimensional space , 2005, Experimental Brain Research.

[10]  M. Cynader,et al.  Abolition of direction selectivity in the visual cortex of the cat. , 1976, Science.

[11]  M. Merzenich,et al.  Role of cat primary auditory cortex for sound-localization behavior. , 1984, Journal of neurophysiology.

[12]  M. Cynader,et al.  Stereoscopic subsystems for position in depth and for motion in depth , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[13]  Auditory cortical neurons in the cat sensitive to the direction of sound source movement. , 1974, Brain research.

[14]  D P Phillips,et al.  Effect of tone-pulse rise time on rate-level functions of cat auditory cortex neurons: excitatory and inhibitory processes shaping responses to tone onset. , 1988, Journal of neurophysiology.

[15]  J. Movshon,et al.  Abolition of visual cortical direction selectivity affects visual behavior in cats , 2004, Experimental Brain Research.

[16]  D. P. Phillips,et al.  Spatial receptive fields in the cat inferior colliculus , 1983, Hearing Research.

[17]  D P Phillips,et al.  Responses of single neurons in physiologically defined primary auditory cortex (AI) of the cat: frequency tuning and responses to intensity. , 1981, Journal of neurophysiology.

[18]  T. Yin,et al.  Binaural interaction in low-frequency neurons in inferior colliculus of the cat. II. Effects of changing rate and direction of interaural phase. , 1983, Journal of neurophysiology.

[19]  L. Aitkin,et al.  Properties of spatial receptive fields in the central nucleus of the cat inferior colliculus. II. Stimulus intensity effects , 1984, Hearing Research.

[20]  Juhani Hyva¨rinen,et al.  Auditory cortical neurons in the cat sensitive to the direction of sound source movement , 1974 .

[21]  Max S. Cynader,et al.  Aural intensity for a moving source , 1991, Hearing Research.

[22]  W. Jenkins,et al.  Sound localization: effects of unilateral lesions in central auditory system. , 1982, Journal of neurophysiology.

[23]  J. Brugge,et al.  Progress in neurophysiology of sound localization. , 1985, Annual review of psychology.

[24]  D. Regan,et al.  Evidence for the existence of neural mechanisms selectively sensitive to the direction of movement in space , 1973, The Journal of physiology.

[25]  G D Pollak,et al.  Binaural response organization within a frequency-band representation of the inferior colliculus: implications for sound localization , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  L. Eisenman,et al.  Neural encoding of sound location: an electrophysiological study in auditory cortex (AI) of the cat using free field stimuli. , 1974, Brain research.

[27]  L. Kitzes,et al.  Patterns of responses of cortical cells to binaural stimulation , 1980, The Journal of comparative neurology.

[28]  G. Henning Detectability of interaural delay in high-frequency complex waveforms. , 1974, The Journal of the Acoustical Society of America.