RESPONSE PROPERTIES OF SINGLE UNITS IN THE DORSAL NUCLEUS OF THE LATERAL LEMNISCUS AND PARALEMNISCAL ZONE OF AN ECHOLOCATING BAT

1. Connectional evidence suggests that the dorsal nucleus of the lateral lemniscus (DNLL) and the paralemniscal one (PL) function as centers for binaural analysis interposed between the superior olivary complex and the midbrain. In addition, the DNLL is known to be a major source of inhibitory input to the midbrain. The aim of this study was to characterize the response properties of neurons in DNLL and PL of the echolocating bat Eptesicus fuscus, a species that utilizes high-frequency hearing and that might be expected to have a large proportion of neurons responsive to interaural differences in sound level. 2. Auditory stimuli were presented monaurally or binaurally to awake animals, and responses of single units were recorded extracellularly with the use of glass micropipettes. 3. Below the ventrolateral border of the inferior colliculus is a region that contains large gamma-aminobutyric acid-positive neurons. On the basis of its immunohistochemical reactivity, this entire region could be considered as DNLL. However, within the area, there was an uneven distribution of binaural responses. Caudally, binaural neurons made up 84% (41/49) of those tested, but rostrally only 29% (6/21 ). For this reason the rostral area is considered as a separate functional subdivision and referred to as the dorsal paralemniscal zone (DPL). PL is located ventral to DPL and medial to the intermediate and ventral nuclei of the lateral lemniscus; in PL 88% (14/16) of neurons were binaural. 4. Most neurons responded only to a contralateral stimulus when sounds were presented monaurally. Out of 49 neurons in DNLL, 42 responded only to a contralateral sound, 1 responded only to an ipsilateral sound, and 6 responded to sound at either ear. In the DPL, all of the 21 neurons tested responded to a contralateral sound and none to an ipsilateral sound. Out of 16 neurons in the PL, 11 responded only to a contralateral sound, 1 responded only to an ipsilateral sound, and 4 responded to sound at either ear. 5. When sounds were presented at both ears simultaneously, several different patterns of binaural interaction occurred. The most common pattern was suppression of the response to sound at one ear by sound at the other ear. In DNLL, 57% (28/49) of neurons showed this type of binaural interaction. Another 10% (5/49) showed facilitation at some interaural level differences and suppression at others, and another 10% (5/49) showed facilitation at some interaural level differences but no suppression. In DPL the only binaural interaction seen was suppression of the response to sound at one ear by sound at the other ear. In PL, 69% (11/16) of neurons showed suppression of the response to sound at one ear by sound at the other ear, and 13% (2/16) showed facilitation at certain interaural level differences but no suppression. 6. Best frequencies of neurons in DNLL, DPL, and PL were distributed throughout the range audible to Eptesicus. In each area, there was an expanded representation of the frequency range between 20 and 30 kHz. The minimum neural thresholds closely matched the minimum behavioral thresholds that have been measured for Eptesicus. No neurons were found to have unusually broad or unusually narrow frequency tuning. 7. There was little evidence of an orderly tonotopic progression in DNLL, DPL, or PL. Instead, neurons with similar best frequencies were clustered together in a mosaic pattern. 8. Most neurons in DNLL, DPL, and PL had low spontaneous activity. Discharge patterns in DNLL were either transient (39%; 16/41) or sustained (58%; 24/41). In DPL the majority of neurons (76%; 16/21) responded transiently. In PL, the most common type of discharge pattern was the sustained type (79%; 11/14). Regularity analysis showed that 12% of neurons in DNLL (5/41) and 38% of neurons in DPL (8/21 ) could be classified as choppers. In response to monaural stimuli, the majority of neurons in all three areas had monotonic rate-level functions. 9. When DNLL neurons were tested with pairs of tones at BF, 30% (7/23) showed a facilitated response to the second of the two tones. Although the facilitation was greatest at certain delays, some facilitation was seen over a period lasting several tens of milliseconds after the first stimulus. This finding suggests that, even at the level of the brain stem, the response of a neuron to a given sound may be influenced by sounds that have occurred previously.