Afferent connections to the dorsal nucleus of the lateral lemniscus of the mustache bat: evidence for two functional subdivisions

Abstract

The dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat, Pteronotus parnellii, was found to consist of two divisions. The neurons in each division were distinguished by their temporal discharge patterns evoked both by tone bursts and sinusoidal amplitude-modulated (SAM) signals. Neurons in the anterior one-third of the DNLL responded to tone bursts with an onset discharge pattern and only phase-locked to SAM signals with low modulation frequencies (< 300 Hz). Neurons in the posterior two-thirds of the DNLL responded to tone bursts with a sustained discharge pattern and phase-locked to SAM signals with much higher modulation frequencies (400-800 Hz). In addition, there was a different frequency representation in the two divisions. The frequency representation in the posterior division was from about 15 to 120 kHz, whereas in the anterior division it was only up to 62 kHz. The physiological differences were further supported by data from experiments that revealed the sources of afferent projections to the two DNLL divisions. Retrograde labeling showed that the afferent projections to the two divisions were from different neuronal populations. Input differences were of two types. Some nuclei projected to one or the other DNLL division, but not to both. For instance, the ventral nucleus of the lateral lemniscus projected predominately to the anterior DNLL and provided little or no inputs to the posterior DNLL, whereas the medial superior olive innervated the posterior but not the anterior DNLL. Other lower nuclei projected to both DNLL divisions. These include the contralateral cochlear nucleus, the ipsi- and contralateral lateral superior olives, the intermediate nucleus of the lateral lemniscus, and the contralateral DNLL. However, the projections to each division of the DNLL originate from different neuronal subpopulations in each lower nucleus. The functional implications of these findings are discussed in the context of the possible impacts that the two DNLL divisions exert on their postsynaptic targets in the inferior colliculus.

Reversible Inactivation of the Dorsal Nucleus of the Lateral Lemniscus Reveals Its Role in the Processing of Multiple Sound Sources in the Inferior Colliculus of Bats

“…They are also the dominant type in the dorsal nucleus of the lateral lemniscus (DNLL), a nucleus the neurons of which are almost exclusively GABAergic (Brugge et al, 1970;Adams and Mugniani, 1984;Covey, 1993; Yang and Pollak, 1994a,b,c;Winer et al, 1995). The DNLL, like the ICc, is one of the principal targets of both the ipsilateral and contralateral LSOs (Glendenning et al, 1981;Ross et al, 1988;Shneiderman et al, 1988Shneiderman et al, , 1999Yang et al, 1996). The DNLL, in turn, sends strong GABAergic projections bilaterally to the ICc (Ross et al, 1988;Shneiderman et al, 1988Shneiderman et al, , 1999Gonzalez-Hernandez et al, 1996;Kelly et al, 1998).…”

Response Properties of Single Units in the Dorsal Nucleus of the Lateral Lemniscus of Decerebrate Cats

“…Principal cells in the medial superior olive (MSO), the lateral superior olive (LSO), and the cochlear nuclei have unique response patterns and are primary sources of ascending inputs to the DNLL (Casseday et al 1988;Glendenning et al 1981;Shneiderman et al 1988;Vater et al 1995;Yang et al 1996). Shneiderman et al (1988) showed that the afferent axons from these sources to the DNLL are distributed in horizontal bands and have a tonotopic organization.…”

“…It receives roughly the same complement of ascending inputs as the IC including projections from the contralateral cochlear nucleus, the ipsilateral medial superior olive, and both lateral superior olives (Casseday et al 1988; Glendenning et al 1981;Shneiderman et al 1988;Vater et al 1995;Yang et al 1996). It also receives a heavy input from the contralateral DNLL by the commissure of Probst (Glendenning et al 1981; Iwahori 1986;Oliver and Shneiderman 1989;Shneiderman et al 1988).…”

“…The physiological response properties of DNLL neurons have been described in a variety of species including cat (Aitkin et al 1970; Brugge et al 1970), horseshoe bat (Metzner and Radtke-Schuller 1987), big brown bat (Covey 1993), mustache bat (Markovitz and Pollak 1993, 1994; Pollak 1994a,b, 1998;Yang et al 1996), rat (Bajo et al 1998 Kelly et al 1998), Mexican free-tailed bat (Bauer et al 2002;Xie et al 2005), gerbil (Siveke et al 2006, and rabbit (Kuwada et al 2006). There is good agreement among these studies that most units in the DNLL show V-shaped excitatory tuning curves for contralateral stimulation and that most units are binaural.…”

“…1993; Kelly and Li 1997; Kidd and Kelly 1996; Li and Kelly 1992; Thornton and Rees 1997). Behavioral studies have shown that lesions of the DNLL or transection of its crossed efferent projections in the commissure of Probst degrade the ability of animals to localize sounds in the horizontal plane (Ito et al 1996;Kelly et al 1996).The physiological response properties of DNLL neurons have been described in a variety of species including cat (Aitkin et al 1970; Brugge et al 1970), horseshoe bat (Metzner and Radtke-Schuller 1987), big brown bat (Covey 1993), mustache bat (Markovitz and Pollak 1993, 1994; Pollak 1994a,b, 1998;Yang et al 1996), rat (Bajo et al 1998 Kelly et al 1998), Mexican free-tailed bat (Bauer et al 2002;Xie et al 2005), gerbil (Siveke et al 2006, and rabbit (Kuwada et al 2006). There is good agreement among these studies that most units in the DNLL show V-shaped excitatory tuning curves for contralateral stimulation and that most units are binaural.…”