Serotonergic innervation of the auditory brainstem of the Mexican free‐tailed bat, Tadarida brasiliensis

Abstract

Anatomical and electrophysiological evidence suggests that serotonin alters the processing of sound in the auditory brainstem of many mammalian species. The Mexican free-tailed bat is a hearing specialist, like other microchiropteran bats. At the same time, many aspects of its auditory brainstem are similar to those in other mammals. This dichotomy raises an interesting question regarding the serotonergic innervation of the bat auditory brainstem: Is the serotonergic input to the auditory brainstem similar in bats and other mammals, or are there specializations in the serotonergic innervation of bats that may be related to their exceptional hearing capabilities? To address this question, we immunocytochemically labeled serotonergic fibers in the brainstem of the Mexican free-tailed bat, Tadarida brasiliensis. We found many similarities in the pattern of serotonergic innervation of the auditory brainstem in Tadarida compared with other mammals, but we also found two striking differences. Similarities to staining patterns in other mammals included a higher density of serotonergic fibers in the dorsal cochlear nucleus and in granule cell regions than in the ventral cochlear nucleus, a high density of fibers in some periolivary nuclei of the superior olive, and a higher density of fibers in peripheral regions of the inferior colliculus compared with its core. The two novel features of serotonergic innervation in Tadarida were a high density of fibers in the fusiform layer of the dorsal cochlear nucleus relative to surrounding layers and a relatively high density of serotonergic fibers in the low-frequency regions of the lateral and medial superior olive.

Serotonin Shifts First-Spike Latencies of Inferior Colliculus Neurons

“…These response characteristics include paradoxical latency shifts, time-intensity trading, and latency-dependent binaural interactions (Kuwada and Yin, 1983;Pollak, 1988;Melssen et al, 1990;Park et al, 1998;Klug et al, 2000). Importantly, the similarities between the IC of free-tailed bats and other mammals extend to the pattern of innervation by serotonergic fibers, which is similar across species (Kaiser and Covey, 1997;Hurley and Thompson, 2001).…”

“…In addition, something that argues that at least some of the effects of serotonin are attributable to modulation of inhibitory transmission is the association of serotonin and GABA in the IC. Both GABAergic puncta (Winer et al, 1995) and serotonergic fibers and varicosities (Klepper and Herbert, 1991;Hurley and Thompson, 2001) are denser in the dorsal region of the IC, in which neurons whose longer latencies are shaped by inhibition are preferentially found . More directly, approximately two-thirds of GABAergic neurons are associated with serotonin receptors in the IC (Peruzzi and Dut, 2004).…”

The serotonin releaser fenfluramine alters the auditory responses of inferior colliculus neurons

“…Within the central nucleus of the IC, serotonergic fibers are denser in the dorsomedial region than in the ventral and lateral regions (Kaiser and Covey 1997;Hurley and Thompson 2001). Thus, one way that the effects of fenfluramine could differ from those of serotonin is in the recording depths or CFs of the neurons it targets.…”

“…This prediction reflects the gradient in the density of serotonergic fibers seen in the central IC of multiple species of mammals, including the Mexican free-tailed bat. In multiple species, serotonergic fibers in the central IC are denser dorsomedially, with regions of lower density ventrally and sometimes laterally (Klepper and Herbert 1991;Kaiser and Covey 1997;Hurley and Thompson 2001). These fibers are both sources of and sinks for serotonin because they house serotonergic reuptake sites as well as sites for serotonin release (Nielsen et al 2006).…”

“…On the other hand, levels of endogenously released serotonin could differ regionally or temporally from those of exogenously applied serotonin. One reason for this is that serotonergic fibers are denser in some regions of the IC than others, such as the dorsal and external cortices, and also in the dorsomedial region of the central nucleus of the IC in some species including the free-tailed bat (Klepper and Herbert 1991;Kaiser and Covey 1997;Hurley and Thompson 2001). This distribution of fibers may also mean that serotonin clearance is more rapid in regions of high release, since serotonin transporters are located on serotonergic fibers (Nielsen et al 2006).…”