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

1991 ◽  
Vol 65 (6) ◽  
pp. 1275-1296 ◽  
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)

Distribution of combination-sensitive neurons in the ventral fringe area of the auditory cortex of the mustached bat

1989 ◽  
Vol 61 (1) ◽  
pp. 202-207 ◽  
Author(s):  
H. Edamatsu ◽  
M. Kawasaki ◽  
N. Suga
Keyword(s):  
Auditory Cortex ◽  
Functional Organization ◽  
Target Range ◽  
Sound Pulse ◽  
Constant Frequency ◽  
Mustached Bat ◽  
Essential Components ◽  
Tritiated Amino Acids ◽  
Pulse Echo ◽  
Echo Delay

1. The orientation sound (pulse) of the mustached bat, Pteronotus parnellii parnellii, consists of long constant-frequency components (CF1-4) and short frequency-modulated components (FM1-4). The auditory cortex of this bat contains several combination-sensitive areas: FM-FM, DF, VA, VF, and CF/CF. The FM-FM area consists of neurons tuned to a combination of the pulse FM1 and the echo FMn (n = 2, 3, or 4) and has an echo-delay (target-range) axis. Our preliminary anatomical studies with tritiated amino acids suggest that the FM-FM area projects to the dorsal fringe (DF) area, which in turn projects to the ventral fringe (VF) area. The aim of our study was to characterize the response properties of VF neurons and to explore the functional organization of the VF area. Acoustic stimuli delivered to the bats were CF tones, FM sounds, and their combinations mimicking the pulse emitted by the mustached bat and the echo. 2. Like the FM-FM and DF areas, the VF area is composed of three types of FM-FM combination-sensitive neurons: FM1-FM2, FM1-FM3, and FM1-FM4. These neurons show little or no response to a pulse alone, echo alone, single CF tone or single FM sound. They do, however, show a strong facilitative response to a pulse-echo pair with a particular echo delay. The essential components in the pulse-echo pair for facilitation are the FM1 of the pulse and the FMn of the echo.(ABSTRACT TRUNCATED AT 250 WORDS)

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

2002 ◽  
Vol 88 (1) ◽  
pp. 172-187 ◽  
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.

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

1991 ◽  
Vol 65 (6) ◽  
pp. 1254-1274 ◽  
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)

Are the initial frequency-modulated components of the mustached bat's biosonar pulses important for ranging?

1991 ◽  
Vol 66 (6) ◽  
pp. 1951-1964 ◽  
Author(s):  
D. C. Fitzpatrick ◽  
N. Suga ◽  
H. Misawa
Keyword(s):  
Maximum Amplitude ◽  
Signal Amplitude ◽  
Frequency Component ◽  
Target Range ◽  
Constant Frequency ◽  
Range Resolution ◽  
Mustached Bat ◽  
Pteronotus Parnellii ◽  
Target Ranging ◽  
The Mean

1. FM-FM neurons in the auditory cortex of the mustached bat, Pteronotus parnellii, are specialized to process target range. They respond when the terminal frequency-modulated component (TFM) of a biosonar pulse is paired with the TFM of the echo at a particular echo delay. Recently, it has been suggested that the initial FM components (IFMs) of biosonar signals may also be important for target ranging. To examine the possible role of IFMs in target ranging, we characterized the properties of IFMs and TFMs in biosonar pulses emitted by bats swung on a pendulum. We then studied responses of FM-FM neurons to synthesized biosonar signals containing IFMs and TFMs. 2. The mustached bat's biosonar signal consists of four harmonics, of which the second (H2) is the most intense. Each harmonic has an IFM in addition to a constant-frequency component (CF) and a TFM. Therefore each pulse potentially consists of 12 components, IFM1-4, CF1-4, and TFM1-4. The IFM sweeps up while the TFM sweeps down. 3. The IFM2 and TFM2 depths (i.e., bandwidths) were measured in 217 pulses from four animals. The mean IFM2 depth was much smaller than the mean TFM2 depth, 2.87 +/- 1.52 (SD) kHz compared with 16.27 +/- 1.08 kHz, respectively. The amplitude of the IFM2 continuously increased throughout its duration and was always less than the CF2 amplitude, whereas the TFM2 was relatively constant in amplitude over approximately three-quarters of its duration and was often the most intense part of the pulse. The maximum amplitude of the IFM2 was, on average, 11 dB smaller than that of the TFM2. Because range resolution increases with depth and the maximum detectable range increases with signal amplitude, the IFMs are poorly suited for ranging compared with the TFMs. 4. FM-FM neurons (n = 77) did not respond or responded very poorly to IFMs with depths and intensities similar to those emitted on the pendulum. The mean IFM2 depth at which a just-noticeable response appeared was 4.48 +/- 1.98 kHz. Only 14% of the pulses emitted on the pendulum had IFM2 depths that exceeded the mean IFM2 depth threshold of FM-FM neurons. 5. Most FM-FM neurons responded to IFMs that had depths comparable with those of TFMs. However, when all parameters were adjusted to optimize the response to TFMs and then readjusted to maximize the response to IFMs, 52% of 27 neurons tested responded significantly better to the optimal TFMs than to the optimal IFMs (P less than 0.05, t test).(ABSTRACT TRUNCATED AT 400 WORDS)

Long delay lines for ranging are created by inhibition in the inferior colliculus of the mustached bat

1995 ◽  
Vol 74 (1) ◽  
pp. 1-11 ◽  
Author(s):  
I. Saitoh ◽  
N. Suga
Keyword(s):  
Auditory Cortex ◽  
Receptor Antagonist ◽  
Inferior Colliculus ◽  
Coincidence Detection ◽  
Central Nucleus ◽  
Gamma Aminobutyric Acid ◽  
Delay Lines ◽  
Mustached Bat ◽  
Gabaa Receptor Antagonist ◽  
Medial Geniculate

1. The central auditory system of the mustached bat has arrays of delay-tuned (FM-FM combination-sensitive) neurons in the inferior colliculus, the medial geniculate body, and the auditory cortex. These neurons are tuned to particular echo delays, i.e., target distances. The neural mechanisms for creating the delay-tuned neurons involve delay lines, coincidence detection, and amplification. We have hypothesized that delay lines longer than 4 ms are created by inhibition occurring in the anterolateral division (ALD) of the central nucleus of the inferior colliculus. If this hypothesis is correct, suppression of inhibition occurring in the ALD must shorten the best delays of the collicular, thalamic, and cortical delay-tuned neurons. The aim of the present study is to test this hypothesis. Responses of single delay-tuned neurons in the FM-FM area of the auditory cortex were recorded with a tungsten-wire microelectrode, and the effects of iontophoretic microinjections of strychnine (STR) and/or bicuculline methiodide (BMI) into the ALD were examined on the responses of these neurons. 2. STR (glycine receptor antagonist) and/or BMI [gamma-aminobutyric acid-A (GABAA) receptor antagonist] injections into the ALD shortened the best delays of delay-tuned neurons in the FM-FM area with little change in their response patterns. The longer the best delay of a delay-tuned neuron, the larger the amount of shortening. 3. Inhibition mediated by glycine receptors plays a larger role in creating delay lines than that mediated by GABAA receptors, because STR and BMI, respectively, shortened the best delay of 91 and 74% of the neurons with best delays longer than 4.5 ms. 4. BMI has no effect on the best delays of delay-tuned neurons that were tuned to echo delays shorter than 4.5 ms. 5. The present data support the hypothesis that long delay lines utilized by delay-tuned neurons are created by inhibition occurring in the ALD of the inferior colliculus. However, the amount of shortening in delay lines by STR and/or BMI was generally smaller than that predicted by a neural network model. Therefore the present study partially answers the questions of where and how long delay lines were created.

Delay lines and amplitude selectivity are created in subthalamic auditory nuclei: the brachium of the inferior colliculus of the mustached bat

1993 ◽  
Vol 69 (5) ◽  
pp. 1713-1724 ◽  
Author(s):  
N. Kuwabara ◽  
N. Suga
Keyword(s):  
Inferior Colliculus ◽  
Subthalamic Nucleus ◽  
Frequency Component ◽  
Nerve Fibers ◽  
Coincidence Detection ◽  
Delay Lines ◽  
Constant Frequency ◽  
Response Latencies ◽  
Mustached Bat ◽  
Species Specific

1. The biosonar pulse of the mustached bat, Pteronotus parnellii parnellii, consists of four harmonics of a constant-frequency component (CF1-4) followed by a frequency-modulated component (FM1-4). FM-FM combination-sensitive neurons in the auditory cortex and the medical geniculate body (MGB) show facilitative responses to certain combinations of FM components in a pulse-echo pair. They are tuned to particular delays of echo FMn (EFMn) (n = 2, 3, or 4) from pulse FM1 (PFM1). The neural mechanisms for creating their response properties involve delay lines, coincidence detection, and multiplication. Coincidence detection and multiplication take place in the MGB. It is not yet known where and how delay lines are created. The first aim of the present studies is to examine whether delay lines are created by subthalamic nuclei. FM-FM neurons are tuned to not only echo delays but also echo amplitudes. Therefore, the second aim of the present studies is to examine the extent to which amplitude selectivity is created by subthalamic nuclei. Responses of single nerve fibers to acoustic stimuli were recorded from the brachium of the inferior colliculus (BIC) using tungsten wire microelectrodes, and their response latencies and best amplitudes were measured. 2. All BIC fibers responded strongly to single tone bursts. No FM-FM combination-sensitive neurons were found in the BIC. The best frequencies of BIC fibers were predominantly within the frequency ranges of four harmonics of the species-specific biosonar pulse. 3. The response latencies of BIC fibers tuned to FM1 were more diverse (3.5-15.0 ms) than those of BIC fibers tuned to FMn (3.8-6.5 ms). This difference in latency distribution was independent of stimulus amplitude. These data are consistent with the theory that delay lines utilized by FM-FM neurons are created by neurons tuned to the "FM1 frequency," and indicate that the delay lines are mostly, if not all, created in a subthalamic nucleus or nuclei. 4. The best amplitudes of BIC fibers tuned to FM1 or CF1 were 63.2 +/- 4.5 (SE) dB SPL, and those of BIC fibers tuned to FMn or CFn were 48.2 +/- 10.7 dB SPL. The distribution of the best amplitudes of BIC fibers were very similar to those of FM-FM and CF/CF neurons in the MGB. These data indicate that the amplitude selectivity of thalamic FM-FM and CF/CF neurons is mainly a product of a subthalamic nucleus or nuclei.(ABSTRACT TRUNCATED AT 400 WORDS)

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

1999 ◽  
Vol 82 (5) ◽  
pp. 2528-2544 ◽  
Author(s):  
Jeffrey J. Wenstrup
Keyword(s):  
Auditory Cortex ◽  
Frequency Tuning ◽  
Medial Geniculate Body ◽  
Reticular Nucleus ◽  
Complex Frequency ◽  
Complex Sounds ◽  
Frequency Bands ◽  
Mustached Bat ◽  
Medial Geniculate ◽  
Spectral Responses

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.

Sign in / Sign up

Export Citation Format

Share Document