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The Journal of Neuroscience, August 5, 2009, 29(31):9725-9739; doi:10.1523/JNEUROSCI.5459-08.2009

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Behavioral/Systems/Cognitive
Spectrotemporal Response Properties of Inferior Colliculus Neurons in Alert Monkey

Huib Versnel,^1,3 Marcel P. Zwiers,^1,2 and A. John van Opstal¹

¹Department of Biophysics and ²Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition, and Behaviour, Radboud University Nijmegen, 6525 EZ Nijmegen, The Netherlands, and ³Department of Otorhinolaryngology, Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, 3508 GA Utrecht, The Netherlands

Correspondence should be addressed to Dr. Huib Versnel, Department of Otorhinolaryngology, Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, P.O. Box 85500, 3508 GA Utrecht, The Netherlands. Email: h.versnel{at}umcutrecht.nl

Because of its central position in the ascending auditory pathway, its large number of converging auditory brainstem inputs, and its fundamental role as a relay to auditory cortex and midbrain superior colliculus, the mammalian inferior colliculus (IC) is regarded pivotal for the integration of acoustic spectral–temporal cues to mediate sound-evoked behavior. However, detailed quantitative analyses of spectrotemporal neural responses are scarce. Moreover, most studies have been performed in anesthetized preparations, and it is unclear how to extrapolate findings to awake and behaving animals. Here, we characterize spectrotemporal receptive fields (STRFs) of single units in alert monkey IC by using a variety of broadband sounds with rippled amplitude spectra. We measured the response sensitivity to the ripple parameters density, (cycles/octave), velocity, w (hertz), and direction selectivity, D. We observed a variety of dynamic STRFs, with a strong preference for low ripple densities, and a generally weak direction selectivity. Most cells preferred dynamic rippled stimuli above pure amplitude modulated noise (i.e., = 0). Half of the cells could be characterized by good spectral–temporal separability, in which the ripple transfer function can be written as T(w, ) = F(w) x G(). Inseparability could be attributed to a difference in responses to up and downward direction with respect to both amplitude and temporal phase. We tested linearity of IC neurons by using the STRF to predict neural responses to natural stimuli and broadband noise and discuss our results in the light of findings obtained from auditory cortex.

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Received Nov. 11, 2008; revised March 13, 2009; accepted June 13, 2009.

Correspondence should be addressed to Dr. Huib Versnel, Department of Otorhinolaryngology, Rudolf Magnus Institute of Neuroscience, University Medical Center Utrecht, P.O. Box 85500, 3508 GA Utrecht, The Netherlands. Email: h.versnel{at}umcutrecht.nl

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