Frequency Organization and Responses to Complex Sounds in the Medial Geniculate Body of the Mustached Bat

Abstract

The auditory cortex of the mustached bat (Pteronotus parnellii) displays some of the most highly developed physiological and organizational features described in mammalian auditory cortex. This study examines response properties and organization in the medial geniculate body (MGB) that may contribute to these features of auditory cortex. About 25% of 427 auditory responses had simple frequency tuning with single excitatory tuning curves. The remainder displayed more complex frequency tuning using two-tone or noise stimuli. Most of these were combination-sensitive, responsive to combinations of different frequency bands within sonar or social vocalizations. They included FM-FM neurons, responsive to different harmonic elements of the frequency modulated (FM) sweep in the sonar signal, and H1-CF neurons, responsive to combinations of the bat's first sonar harmonic (H1) and a higher harmonic of the constant frequency (CF) sonar signal. Most combination-sensitive neurons (86%) showed facilitatory interactions. Neurons tuned to frequencies outside the biosonar range also displayed combination-sensitive responses, perhaps related to analyses of social vocalizations. Complex spectral responses were distributed throughout dorsal and ventral divisions of the MGB, forming a major feature of this bat's analysis of complex sounds. The auditory sector of the thalamic reticular nucleus also was dominated by complex spectral responses to sounds. The ventral division was organized tonotopically, based on best frequencies of singly tuned neurons and higher best frequencies of combination-sensitive neurons. Best frequencies were lowest ventrolaterally, increasing dorsally and then ventromedially. However, representations of frequencies associated with higher harmonics of the FM sonar signal were reduced greatly. Frequency organization in the dorsal division was not tonotopic; within the middle one-third of MGB, combination-sensitive responses to second and third harmonic CF sonar signals (60-63 and 90-94 kHz) occurred in adjacent regions. In the rostral one-third, combination-sensitive responses to second, third, and fourth harmonic FM frequency bands predominated. These FM-FM neurons, thought to be selective for delay between an emitted pulse and echo, showed some organization of delay selectivity. The organization of frequency sensitivity in the MGB suggests a major rewiring of the output of the central nucleus of the inferior colliculus, by which collicular neurons tuned to the bat's FM sonar signals mostly project to the dorsal, not the ventral, division. Because physiological differences between collicular and MGB neurons are minor, a major role of the tecto-thalamic projection in the mustached bat may be the reorganization of responses to provide for cortical representations of sonar target features.

Spectral Integration in A1 of Awake Primates: Neurons With Single- and Multipeaked Tuning Characteristics

“…Enhanced neural responses by two tones have been observed in some subcortical nuclei, for example, in ventral cochlear nucleus (VCN) of guinea pigs (Jiang et al 1996;Winter and Palmer 1995), lateral lemniscus, IC and MGB in bats Wenstrup 1999, 2001;Wenstrup 1999). However, such enhancement appears to be less promi-nent than that observed in A1.…”

“…In some mammalian species such as bats, a class of specialized neurons was found in the auditory cortex (Suga et al 1978(Suga et al , 1983 and subcortical nuclei (Leroy and Wenstrup 2000;Olsen and Suga 1991;Wenstrup 1999) that responds optimally to specific combinations of spectral components in sonar signals that are harmonically related. These neurons have been referred to as "combination-sensitive" neurons.…”

Subcortical processing in auditory communication

“…Evidence in this direction comes from the observation that both the IC and the MGB are sensitive to basic spectral features and their variations over time (Nelken, 2008;Baumann et al, 2011), as well as to specific combinations of spectral features (Kanwal and Rauschecker, 2007). Furthermore, the MGB is responsive to complex sounds (Wenstrup, 1999), and its activity is modulated by the task (e.g. it shows adaptation to repeated speech recognition, Von Kriegstein et al, 2008), as well as by the context (e.g.…”

“…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.…”

Reorganization of the auditory cortex specialized for echo-delay processing in the mustached bat

“…In the mustached bat, an array of neurons tuned to certain echo delays (i.e., the time interval between two sounds) has been found in the FM-FM area of the AC (22-26) (Fig. 1 A) and the subcortical auditory nuclei (24,(27)(28)(29). Electric stimulation of cortical delay-tuned neurons evokes centrifugal best delay (BD) shifts of thalamic and collicular delay-tuned neurons (29).…”