The monaural nuclei of the lateral lemniscus in an echolocating bat: parallel pathways for analyzing temporal features of sound

Abstract

In echolocating bats, three cell groups in the lateral lemniscus are conspicuous for their large size and high degree of differentiation. These cell groups are the intermediate nucleus (INLL), columnar nucleus (VNLLc), and multipolar cell area (VNLLm). All receive projections from the contralateral cochlear nucleus. Previous anatomical studies suggest the hypothesis that these nuclei are important for analyzing the temporal structure of sound. To investigate this possibility, we recorded responses of single units in the INLL, VNLLc, and VNLLm of Eptesicus fuscus. The results show that each cytoarchitectural division contains a complete tonotopic representation. Certain response properties are common to all three nuclei. First, virtually all units are monaural. Second, all are broadly tuned to frequency; their average Q10dB value of 9.1 is considerably lower than values measured in the inferior colliculus of Eptesicus. Third, most units have little or no spontaneous activity. Fourth, all have short integration times, responding robustly to stimuli less than 5 msec in duration. The broad tuning, lack of spontaneous activity, and short integration time all make these neurons well suited for the accurate encoding of temporal information. Although there are many similarities, there are also important differences among nuclei. The clearest evidence of specialization is in VNLLc. Neurons here are more broadly tuned than those in INLL or VNLLm, have no spontaneous activity, and always respond with one spike per stimulus. The latency of the spike is precisely locked to the stimulus onset, with variability from trial to trial as low as 0.03 msec. In addition, the latency remains constant over large variations in frequency or intensity. In INLL and VNLLm, response patterns are about equally distributed between tonic, chopping, and phasic; there are no single-spike constant-latency responses of the type seen in VNLLc, although some choppers and pausers do respond with constant first-spike latency. The results indicate that VNLLc is specialized to encode very precisely the onset of sound; the other nuclei may encode ongoing properties of a sound.

Organization of projection from brainstem auditory nuclei to the inferior colliculus of Japanese house bat (Pipistrellus abramus)

“…However, it has been shown that tonotopic organization of monaural nuclei of the lateral lemniscus in big brown bat ( Epitesicus fuscus ) is complicated (Covey & Casseday, 1991), and it is difficult to conclude about the tonotopic organization in the NLL of Japanese house bat. Finer injection with best frequency identification is necessary to solve the issue.…”

“…To analyze the echoes and pulses themselves, auditory nuclei of bats are remarkably hypertrophied (Zook & Casseday, 1982a), and show specialization related to echolocation (Covey & Casseday, 1995), which is obvious in the medial superior olive (MSO) of the superior olivary complex (SOC) (Casseday, Covey, & Vater, 1988; Covey, Vater, & Casseday, 1991; Grothe, Park, & Schuller, 1997; Grothe, Schweizer, Pollak, Schuller, & Rosemann, 1994) and monaural nuclei of the lateral lemniscus, namely intermediate nucleus (ILL) and compact and multipolar cell divisions of ventral nucleus (VLLc and VLLm) (Covey & Casseday, 1991). Lower brainstem nuclei, namely, cochlear nuclei (CN), SOC, and nuclei of the lateral lemniscus (NLL), analyze specific features of sound and send the analyzed information to the inferior colliculus (IC), which is the largest nuclei in entire subcortical auditory system (Ito, Bishop, & Oliver, 2016).…”

Large Somatic Synapses on Neurons in the Ventral Lateral Lemniscus Work in Pairs

“…Along the same line, neurons of the octopus cell area diverge on several VNLL neurons (Covey and Casseday, 1986;Vater and Feng, 1990;Adams, 1997;Schofield and Cant, 1997). Finally, neurons in the VNLL appear to inherit physiological properties from neurons in the octopus cell area as both are broadly tuned and preferentially spike to sound onsets (Godfrey et al, 1975;Rhode et al, 1983;Covey and Casseday, 1991;Smith et al, 2005;Zhang and Kelly, 2006).…”

Response patterns to sound associated with labeled globular/bushy cells in cat

“…MNTB neurons also project to the VNLL, where they terminate in calyceal-like endings (Adams and Wenthold, 1987). VNLL is part of a monaural ascending system purported to play a role in temporal processing of signals (Covey and Casseday, 1991).…”