Response Properties of Neighboring Neurons in the Auditory Midbrain for Pure-Tone Stimulation: A Tetrode Study

Abstract

Seshagiri CV, Delgutte B. Response properties of neighboring neurons in the auditory midbrain for pure-tone stimulation: a tetrode study. J Neurophysiol 98: 2058J Neurophysiol 98: -2073J Neurophysiol 98: , 2007. First published August 1, 2007; doi:10.1152/jn.01317.2006. The complex anatomical structure of the central nucleus of the inferior colliculus (ICC), the principal auditory nucleus in the midbrain, may provide the basis for functional organization of auditory information. To investigate this organization, we used tetrodes to record from neighboring neurons in the ICC of anesthetized cats and studied the similarity and difference among the responses of these neurons to pure-tone stimuli using widely used physiological characterizations. Consistent with the tonotopic arrangement of neurons in the ICC and reports of a threshold map, we found a high degree of correlation in the best frequencies (BFs) of neighboring neurons, which were mostly Ͻ3 kHz in our sample, and the pure-tone thresholds among neighboring neurons. However, width of frequency tuning, shapes of the frequency response areas, and temporal discharge patterns showed little or no correlation among neighboring neurons. Because the BF and threshold are measured at levels near the threshold and the characteristic frequency (CF), neighboring neurons may receive similar primary inputs tuned to their CF; however, at higher levels, additional inputs from other frequency channels may be recruited, introducing greater variability in the responses. There was also no correlation among neighboring neurons' sensitivity to interaural time differences (ITD) measured with binaural beats. However, the characteristic phases (CPs) of neighboring neurons revealed a significant correlation. Because the CP is related to the neural mechanisms generating the ITD sensitivity, this result is consistent with segregation of inputs to the ICC from the lateral and medial superior olives.

Monopolar Intracochlear Pulse Trains Selectively Activate the Inferior Colliculus

“…9). This same pattern also held true for bipolar and acoustic stimulation and is consistent with previous studies of IC responses to acoustic tones (Rose et al 1963;Aitkin et al 1994;Harris et al 1997;Seshagiri and Delgutte 2007) and electrical pulse trains (Bierer et al 2010). Interestingly, in the present study, onset responses to acoustic and electrical stimuli could be quite broad, extending over several millimeters (or several octaves) of the IC tonotopic axis at higher levels, whereas sustained responses covered a much narrower extent (for acoustic stimuli at 60 dB SPL the extent was FIG.…”

Three-dimensional localization of neurons in cortical tetrode recordings

“…After correcting for the 10 -15% excess by which the dipole model tends to overestimate source distance (Mechler and Victor 2011), and estimating separately for different contact separation (⌬s) on the Thomas tetrodes, the R 50 recording radius was Ϸ80 -85 m for the smaller and intermediate tetrodes (⌬s ϭ 29 m and ⌬s 38 m, respectively) and Ϸ95-100 m for the larger tetrode (⌬s ϭ 45 m). These ranges of tetrode sensitivity are generally consistent with the characteristic linear span (can be Ͼ200 m) over which polytrodes reportedly register signals from cortical single units (Blanche et al 2005;Drake et al 1988) but remain significantly larger than the Ϸ50-to 70-m recording radii reported for twisted wire tetrodes (Gray et al 1995;Henze et al 2000;Maldonado et al 1997;Seshagiri and Delgutte 2007). There are several reasons the estimates can differ; the most important ones are difference in source model type, probe size (contact separation), and neuron size.…”

“…We have found that the recording volume (radius Ϸ100 m) of a stationary tetrode was much larger than its most frequently quoted antecedents (Ϸ60 m) (Gray et al 1995;Henze et al 2000;Maldonado et al 1997;Seshagiri and Delgutte 2007), that within this volume the isolation sensitivity was approximately homogeneous and the isolated fraction of neurons small (Ϸ0.3%), and that the neurons could be localized with a precision that was much smaller (radius Ϸ50 m) than the entire recording volume. This improved precision for localizing a cell requires that it is recorded by the tetrode in more than one position.…”

“…Gray's R exp Ϸ 65 m recording radius is defined in cat area 17, and near their noise threshold, and was obtained by triangulation based on a phenomenological approximation of extracellular potentials (Bartho et al 2004;Buzsaki 2004;Gray et al 1995;Maldonado et al 1997;Seshagiri and Delgutte 2007). The value of R exp reported by Gray et al is consistent with a ⌬s ϭ 25 m effective contact separation on their wire tetrodes (Chelaru and Jog 2005;Jog et al 2002).…”

Auditory Midbrain Implant: A Review

“…Considering that frequency is coded along one dimension of the ICC, this raises the possibility that temporal features may be coded spatially along the isofrequency laminae. There are animal studies that have shown that various temporal features, such as periodicity and latencies, are coded systematically along these ICC laminae Schreiner & Langner, 1988) under certain stimulus conditions (Krishna & Semple, 2000;Seshagiri & Delgutte, 2007). Thus, it is possible that we may need to stimulate along the frequency axis of the ICC to transmit varying pitch percepts and across different regions within these isofrequency laminae to transmit sufficient temporal information.…”