The neurons of the medial geniculate body in the mustached bat (Pteronotus parnellii)

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.

Download Full-text

Directional Selectivity for FM Sweeps in the Suprageniculate Nucleus of the Mustached Bat Medial Geniculate Body

Journal of Neurophysiology ◽

10.1152/jn.00966.2001 ◽

2002 ◽

Vol 88 (1) ◽

pp. 172-187 ◽

Cited By ~ 21

Author(s):

William E. O'Neill ◽

W. Owen Brimijoin

Keyword(s):

Medial Geniculate Body ◽

Sweep Rate ◽

Spike Count ◽

Directional Selectivity ◽

Constant Frequency ◽

Preferred Direction ◽

Mustached Bat ◽

Medial Geniculate ◽

Modulation Rate ◽

Communication Calls

Mustached bats emit echolocation and communication calls containing both constant frequency (CF) and frequency-modulated (FM) components. Previously we found that 86% of neurons in the ventral division of the external nucleus of the inferior colliculus (ICXv) were directionally selective for linear FM sweeps and that selectivity was dependent on sweep rate. The ICXv projects to the suprageniculate nucleus (Sg) of the medial geniculate body. In this study, we isolated 37 single units in the Sg and measured their responses to best excitatory frequency (BEF) tones and linear 12-kHz upward and downward FM sweeps centered on the BEF. Sweeps were presented at durations of 30, 12, and 4 ms, yielding modulation rates of 400, 1,000, and 3,000 kHz/s. Spike count versus level functions were obtained at each modulation rate and compared with BEF controls. Sg units responded well to both tones and FM sweeps. BEFs clustered at 58 kHz, corresponding to the dominant CF component of the sonar signal. Spike count functions for both tones and sweeps were predominantly non-monotonic. FM directional selectivity was significant in 53–78% of the units, depending on modulation rate and level. Units were classified as up-selective (52%), down-selective(24%), or bi-directional ( non-selective, 16%); a few units (8%) showed preferences that were either rate-or level-dependent. Most units showed consistent directional preferences at all SPLs and modulation rates tested, but typically showed stronger selectivity at lower sweep rates. Directional preferences were attributable to suppression of activity by sweeps in the non-preferred direction (∼80% of units) and/or facilitation by sweeps in the preferred direction (∼20–30%). Latencies for BEF tones ranged from 4.9 to 25.7 ms. Latencies for FM sweeps typically varied linearly with sweep duration. Most FM latency-duration functions had slopes ranging from 0.4 to 0.6, suggesting that the responses were triggered by the BEF. Latencies for BEF tones and FM sweeps were significantly correlated in most Sg units, i.e., the response to FM was temporally related to the occurrence of the BEF in the FM sweep. FM latency declined relative to BEF latency as modulation rate increased, suggesting that at higher rates response is triggered by frequencies in the sweep preceding the BEF. We conclude that Sg and ICXv units have similar, though not identical, response properties. Sg units are predominantly upsweep selective and could respond to either or both the CF and FM components in biosonar signals in a number of echolocation scenarios, as well as to a variety of communication sounds.

Download Full-text

Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of relative velocity information

Journal of Neurophysiology ◽

10.1152/jn.1991.65.6.1254 ◽

1991 ◽

Vol 65 (6) ◽

pp. 1254-1274 ◽

Cited By ~ 78

Author(s):

J. F. Olsen ◽

N. Suga

Keyword(s):

Doppler Shift ◽

Cortical Neurons ◽

Medial Geniculate Body ◽

Distance Information ◽

Tuning Curves ◽

Mustached Bat ◽

Medial Geniculate ◽

Velocity Information ◽

Pulse Echo ◽

Echo Delay

1. Orientation sounds (pulses) emitted by the mustached bat (Pteronotus parnellii) consist of up to four harmonics (H1-4); each harmonic contains a constant frequency (CF) component and a terminal frequency modulated (FM) component, so that there are eight components in total (CF1-4 and FM1-4). By referring the echo from a target to the emitted pulse, the mustached bat derives velocity information from Doppler shift and distance information from echo delay. In this study, the responses of single neurons in the medial geniculate body (MGB) to synthetic biosonar signals were investigated. Stimuli consisted of CF, FM, and CF-FM sounds. Paired CF-FM sounds were used to mimic any two harmonics of pulse-echo pairs. The dorsal and medial divisions of the MGB were found to contain combination-sensitive neurons. These neurons responded poorly to individual sounds regardless of frequency and amplitude and were facilitated by paired sounds presented at particular frequencies, amplitudes and inter-component intervals (simulated echo delay). Combination-sensitive neurons were tuned to the frequencies that characterize particular components of natural biosonar signals and were classified according to the components of pulse-echo pairs that best matched the spectral selectivity of the neuron. Two classes of combination-sensitive neurons were found, CF/CF and FM-FM. This paper focuses on CF/CF combination-sensitive neurons, which extract velocity information from paired CF components, and on CF2 and CF3 neurons, which, although not combination-sensitive, are tuned to the frequencies of the CF2 and CF3 components of biosonar signals. 2. CF2 and CF3 neurons were sharply tuned in frequency. The best frequencies of the most sharply tuned CF2 neurons were all approximately equal to 61.17 kHz (SD = 370 Hz), which closely matches the frequency at which P. parnellii stabilizes the CF2 component of an echo when compensating for Doppler shift. Thus CF2 neurons are specialized for a fine analysis of Doppler-compensated echoes. 3. Tuning curves of CF2 and CF3 neurons remained narrow regardless of stimulus level. When compared at high stimulus levels (30 and 50 dB above minimum threshold), bandwidths of tuning curves of CF2 and CF3 neurons were much smaller than those of peripheral auditory neurons turned to CF2 or CF3 frequencies but were about the same as those of cortical neurons tuned to CF2 or CF3 frequencies. Thus the sharpening of neural tuning curves by the bat's central auditory system occurs within or before the MGB.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text

Corticofugal Amplification of Facilitative Auditory Responses of Subcortical Combination-Sensitive Neurons in the Mustached Bat

Journal of Neurophysiology ◽

10.1152/jn.1999.81.2.817 ◽

1999 ◽

Vol 81 (2) ◽

pp. 817-824 ◽

Cited By ~ 42

Author(s):

Jun Yan ◽

Nobuo Suga

Keyword(s):

Cortical Neurons ◽

Medial Geniculate Body ◽

Inhibitory Effect ◽

Physiological Data ◽

Excitatory Effect ◽

Complex Sounds ◽

Auditory Responses ◽

Mustached Bat ◽

Medial Geniculate ◽

Excitatory Responses

Corticofugal amplification of facilitative auditory responses of subcortical combination-sensitive neurons in the mustached bat. Recent studies on the bat’s auditory system indicate that the corticofugal system mediates a highly focused positive feedback to physiologically “matched” subcortical neurons, and widespread lateral inhibition to physiologically “unmatched” subcortical neurons, to adjust and improve information processing. These findings have solved the controversy in physiological data, accumulated since 1962, of corticofugal effects on subcortical auditory neurons: inhibitory, excitatory, or both (an inhibitory effect is much more frequent than an excitatory effect). In the mustached bat, Pteronotus parnellii parnellii, the inferior colliculus, medial geniculate body, and auditory cortex each have “FM-FM” neurons, which are “combination-sensitive” and are tuned to specific time delays (echo delays) of echo FM components from the FM components of an emitted biosonar pulse. FM-FM neurons are more complex in response properties than cortical neurons which primarily respond to single tones. In the present study, we found that inactivation of the entire FM-FM area in the cortex, including neurons both physiologically matched and unmatched with subcortical FM-FM neurons, on the average reduced the facilitative responses to paired FM sounds by 82% for thalamic FM-FM neurons and by 66% for collicular FM-FM neurons. The corticofugal influence on the facilitative responses of subcortical combination-sensitive neurons is much larger than that on the excitatory responses of subcortical neurons primarily responding to single tones. Therefore we propose the hypothesis that, in general, the processing of complex sounds by combination-sensitive neurons more heavily depends on the corticofugal system than that by single-tone sensitive neurons.

Download Full-text

Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of target range information

Journal of Neurophysiology ◽

10.1152/jn.1991.65.6.1275 ◽

1991 ◽

Vol 65 (6) ◽

pp. 1275-1296 ◽

Cited By ~ 113

Author(s):

J. F. Olsen ◽

N. Suga

Keyword(s):

Stimulus Frequency ◽

Medial Geniculate Body ◽

Neural Mechanism ◽

Coincidence Detection ◽

Target Range ◽

Time Interval ◽

Constant Frequency ◽

Mustached Bat ◽

Medial Geniculate ◽

Pulse Echo

1. Delay-tuned combination-sensitive neurons (FM-FM neurons) have been discovered in the dorsal and medial divisions of the medial geniculate body (MGB) of the mustached bat (Pteronotus parnellii). In this paper we present evidence for a thalamic origin for FM-FM neurons. Our examination of the response properties of FM-FM neurons indicates that the neural mechanism of delay-tuning depends on coincidence detection and involves an interaction between neural inhibition and excitation. 2. The biosonar pulse (P) and its echo (E) produced and heard by the mustached bat consist of four harmonics; each harmonic contains a constant frequency (CF) component and a frequency modulated (FM) component. Thus the pulse-echo pair contains eight CF components (PCF1-4, ECF1-4) and eight FM components (PFM1-4, EFM1-4). The stimuli used in this study consisted of CF, FM, and CF-FM sounds: paired CF-FM sounds were used to simulate any two harmonics of pulse-echo pairs. The responses of FM-FM neurons in the MGB were recorded extracellularly. We found that FM-FM neurons respond poorly or not at all to single sounds, respond strongly to paired sounds, and are tuned to the frequency and amplitude of each sound of the pair and to the time interval separating them (simulated echo delay). 3. All FM-FM neurons are facilitated by paired FM sounds and most are facilitated by paired CF sounds. Best facilitative frequencies measured with paired CF sounds fall outside the frequency ranges of the CF components of biosonar signals, whereas best facilitative frequencies measured with paired FM sounds fall within the frequency ranges of the FM components of biosonar signals. Thus FM-FM neurons are expected to respond selectively to combinations of FM components in biosonar signals. The FM components of pulse-echo pairs essential to facilitate FM-FM neurons are the FM component of the fundamental of the pulse (PFM1) in combination with the FM component of the second, third, or fourth harmonic of an echo (EFM2, EFM3, EFM4; collectively, EFMn). 4. The frequency combinations to which FM-FM neurons are tuned reflect small deviations from the harmonic relationship such as occurs in combinations of FM components from pulses and Doppler-shifted echoes. Compared with CF/CF neurons, however, FM-FM neurons are broadly tuned to stimulus frequency. Thus FM-FM neurons are Doppler-shift tolerant and relatively unspecialized for processing velocity information in the frequency domain.(ABSTRACT TRUNCATED AT 400 WORDS)

Download Full-text