The columnar region of the ventral nucleus of the lateral lemniscus in the big brown bat (Eptesicus fuscus): synaptic arrangements and structural correlates of feedforward inhibitory function

Abstract.

Neurons of the columnar region of the ventral nucleus of the lateral lemniscus of Eptesicus fuscus respond with high-precision constant-latency responses to sound onsets and possess remarkably broad tuning. To study the synaptic basis for this specialized monaural auditory processing and to elucidate the excitatory or inhibitory nature of the input and output circuitry, we have used classical transmission electron microscopy, and postembedding immunocytochemistry for gamma aminobutyric acid (GABA) and glycine on serial semithin sections. The dominant putatively excitatory perisomatic input is provided by large calyx-like terminals that possess round synaptic vesicles and asymmetric synaptic contacts. Additionally, calyces contact the dendrites of neighboring neurons. Putatively inhibitory small boutons possess pleomorphic or flattened synaptic vesicles and symmetrical contacts and are sparsely distributed on somata and dendrites. Almost all neurons are glycine-immunoreactive. There is a moderate amount of glycine-immunoreactive puncta; GABA-immunoreactive puncta are rare. This suggests that (1) there is a fast robust excitatory synaptic input via calyx-like perisomatic endings, (2) calyx-like endings distribute frequency-specific excitatory input across isofrequency sheets by virtue of parallel synapses to somata and adjacent dendrites, and thus, dendritic integration may contribute to the broadening of frequency tuning, (3) the columnar region forms an inhibitory glycinergic feedforward relay in the ascending auditory pathway, a relay that is probably involved in creating filters for time-varying signals.