AZIMUTHAL RECEPTIVE-FIELDS ARE SHAPED BY GABAERGIC INHIBITION IN THE INFERIOR COLLICULUS OF THE MOUSTACHE BAT

1. In this study we examine the effects of GABAergic inhibition on the response properties and the constructed azimuthal receptive fields of 54 excitatory/inhibitory (EI) neurons tuned to 60 kHz in the inferior colliculus of the mustache bat. The constructed azimuthal receptive f ields predict the spike counts that would be evoked by different inten sities of 60-kHz sounds presented from each of 13 azimuthal locations in the frontal sound field. 2. Action potentials were recorded with a micropipette attached to a multibarrel glass electrode. Bicuculline, a n antagonist specific for gamma-aminobutyric acid-A (GABA(A)) receptor s, was iontophoretically applied through the multibarrel electrode. Bo th monaural and binaural response properties were initially recorded a t a variety of interaural intensity disparities (IIDs) and absolute in tensities, and the same response properties were subsequently assessed while GABAergic inhibition was blocked by bicuculline. Azimuthal rece ptive fields both before and during the application of bicuculline wer e constructed from response properties obtained with earphones after c orrecting for the directional properties of the ear and the IIDs gener ated by 60-kHz sounds presented from a variety of azimuthal locations. 3. Bicuculline had virtually no effect on either the monaural or bina ural properties of 19 cells (35%). The constructed azimuthal receptive fields of these cells were also unaffected by bicuculline. Presumably the properties of these cells were formed in a lower nucleus, most li kely the contralateral lateral superior olive (LSO), and were imposed on the collicular cell via the crossed projection from the LSO to the inferior colliculus, which is known to be excitatory. 4. In more than half of the neurons (65%) GABAergic inhibition influenced one or more features of the cell's response properties and thus its azimuthal rece ptive field. Some response properties were formed in the colliculus th rough GABAergic inhibition, whereas others appear to have been shaped initially in a lower nucleus and then further modified by GABAergic in hibition in the inferior colliculus. Moreover, a number of features of GABAergic inhibition that acted on inferior collicular cells were evo ked by stimulation of the contralateral (excitatory) ear, whereas othe r features were influenced by stimulation of the ipsilateral (inhibito ry) ear. 5. In 20 cells (37%) blocking GABAergic inhibition reduced or abolished the inhibition evoked by the ipsilateral ear. The receptive fields of cells in which the ipsilaterally evoked inhibition was redu ced by bicuculline expanded further into the ipsilateral sound field t han they did before bicuculline. Furthermore, the border separating th e locations from which sound could evoke responses and those from whic h sounds failed to evoke responses was not as sharply defined with bic uculline as it was before the application of the drug. Cells in which the ipsilaterally evoked inhibition was abolished by bicuculline were rendered monaural. Their receptive fields expanded such that they enco mpassed the entire frontal sound field. 6. In six cells (11%) the ipsi lateral inhibition was neither reduced in strength nor abolished by bi cuculline, but rather bicuculline changed the IID at which the spike c ount was reduced by 50%. In these cells the border in the receptive fi eld separating the locations from which sound could evoke responses an d those from which sounds failed to evoke responses remained as sharp with bicuculline as it did before bicuculline. However, the location o f the border shifted, thereby causing an expansion of the receptive fi eld into the ipsilateral sound field. 7. One of the most interesting f indings was the influence of blocking GABAergic inhibition on facilita ted EI cells (9 of 54, 17%). The IID functions of these cells differed from other EI cells in that when progressively increasing intensities were presented to the ipsilateral ear, the spike counts of these cell s first increased above that evoked by the contralateral ear alone and then the spike counts declined with yet higher ipsilateral intensitie s. The azimuthal receptive fields of these cells were selective for a small region of space near the midline. In five of the nine facilitate d EI cells, blocking GABAergic inhibition eliminated the ''facilitatio n'' (the increase in spike count due to an increase in intensity at th e ipsilateral ear) in their IID functions. Bicuculline correspondingly eliminated the focal regions of their receptive fields and changed th eir receptive fields into ones that resembled those of a regular EI ne uron. 8. The variety of bicuculline-induced effects presumably reflect s a mixing and matching of the various excitatory and GABAergic projec tions that converge on individual binaural cells to shape one or anoth er azimuthal receptive field type. We propose that each modification o f an azimuthal receptive field may be a consequence of the GABAergic p rojection from a particular lower auditory nucleus. Furthermore, we su ggest that the GABAergic projections from the contralateral dorsal nuc lei of the lateral lemniscus (DNLL) are probably involved in shifting the 50% points of the IID functions in some cells. In other cells, in which the ipsilaterally evoked inhibition was reduced or abolished by bicuculline, the contralateral DNLL most likely was the source of the inhibition. We also suggest that for those EI cells in which the facil itation was eliminated by bicuculline, the ipsilateral DNLL probably p rovided the GABAergic inhibition that was responsible for the facilita tion.