Auditory Responses in the Cochlear Nucleus of Awake Mustached Bats: Precursors to Spectral Integration in the Auditory Midbrain

Abstract

In the cochlear nucleus (CN) of awake mustached bats, single- and two-tone stimuli were used to examine how responses in major CN subdivisions contribute to spectrotemporal integrative features in the inferior colliculus (IC). Across CN subdivisions, the proportional representation of frequencies differed. A striking result was the substantial number of units tuned to frequencies <23 kHz. Across frequency bands, temporal response patterns, latency, and spontaneous discharge differed. For example, the 23- to 30-kHz representation, which comprises the fundamental of the sonar call, had an unusually high proportion of units with onset responses (39%) and low spontaneous rates (53%). Units tuned to 58-59 kHz, corresponding to the sharply tuned cochlear resonance, had slightly but significantly longer latencies than other bands. In units tuned to frequencies >30 kHz, 31% displayed a secondary excitatory peak, usually between 10 and 22 kHz. The secondary peak may originate in cochlear mechanisms for some units, but in others it may result from convergent input onto CN neurons. In 20% of units tested with two-tone stimuli, suppression of best frequency (BF) responses was tuned at least an octave below BF. These properties may underlie similar IC responses. However, other forms of spectral interaction present in IC were absent in CN: we found no facilitatory combination-sensitive interactions and very few combination-sensitive inhibitory interactions of the dominant IC type in which inhibition was tuned to 23-30 kHz. Such interactions arise above CN. Distinct forms of spectral integration thus originate at different levels of the ascending auditory pathway.

Subcortical processing in auditory communication

“…It is comprised of diverse and highly specialised neuronal populations (Ram on y Cajal c.1900;Lorente de N o, 1933Lorente de N o, , 1981 differing in morphology (Harrison and Warr, 1962;Osen, 1969a;and 1969b;Brawer et al, 1974;Heiman-Patterson and Strominger, 1985;Adams, 1986), response properties (Pfeiffer and Kiang, 1965;Pfeiffer, 1966;Evans and Nelson, 1973;Shofner and Young, 1985;Blackburn and Sachs, 1989;Winter and Palmer, 1990;Marsh et al, 2006), and connectivity with the auditory nerve (Liberman, 1991(Liberman, , 1993. Each neuronal population in the CN exhibits distinct projections (summarised in Cant and Benson, 2003), some ipsilateral (Cant and Casseday, 1986), others contralateral (Warr, 1966(Warr, , 1969Winer and Schreiner, 2005), reflecting the distinct functions of the CN anteroventral (involved in sound localisation) and posteroventral regions (involved in sound discrimination) (Eggermont, 2001).…”

“…Despite inter-individual differences, the converging evidence (reviewed above) indicates that neurons in the subcortical pathway e especially in IC and MGB e respond selectively to features in vocalisations (e.g. Wenstrup, 1999;Marsh et al, 2006;Holmstrom et al, 2007;Portfors et al, 2009;Pollak, 2011Pollak, , 2012, and that some of these features (e.g. frequency modulation, Andoni andPollak 2007, Pollak et al, 2011) are known to affect the meaning of vocalisations by signalling affective or emotional states.…”

Glycinergic “Inhibition” Mediates Selective Excitatory Responses to Combinations of Sounds

“…However, this mechanism is challenged by delay tuning of some combination- sensitive neurons, for which low-frequency excitation is delayed by Ͼ30 ms. Such delays are not present in the response latencies of afferent input to IC (Haplea et al, 1994;Klug et al, 2000;Portfors and Wenstrup, 2001;Marsh et al, 2006). Even if lowfrequency inputs are located on distal dendrites, it is not clear how passive electrical properties could create such delays.…”

Postnatal Maturation of Primary Auditory Cortex in the Mustached Bat, Pteronotus parnellii

“…This interpretation favoring immature CF2 neurons as source of the low-frequency tails in anterior cortical locations, however, has to be treated with caution. From the cochlear nucleus of adult mustached bats, it is known that comparable low-frequency tails are not only found for CF2 neurons but also for neurons with higher BFs (Marsh et al 2006). Therefore it is also possible that the cortical low-frequency tails are from more anterior high-frequency regions (AIa).…”