Multiple mechanisms shape selectivity for FM sweep rate and direction in the pallid bat inferior colliculus and auditory cortex

The inferior colliculus (IC) of the pallid bat has a large percentage of neurons that respond selectively to the rate and direction of the bat's echolocation pulse, a downward FM sweep. Three underlying mechanisms have been previously described. Here we describe a fourth mechanism, facilitation, that shapes selectivity for both sweep rate and direction. The neurons studied are termed FM specialists, because they do not respond to tones. Most were selective for the downward sweep direction, and this preference was expressed even when presented with narrowband, 1 kHz sweeps that crossed only a fraction of their excitatory receptive fields. This selectivity was also expressed in response to two tones delayed in time, termed two-tone facilitation (TTF). Direction-selective neurons showed a greatly facilitated response when a higher-frequency tone preceded a lower-frequency tone, simulating conditions in a downward sweep. The degree of temporal asymmetry in facilitation accurately predicted direction selectivity. When the spectral difference between the two tones was increased, the best delay also increased and could be used to predict a neuron's preferred sweep rate. To determine whether TTF alone created rate and direction selectivity, low- and high-frequency inhibitory sidebands, which can also shape selectivity, were eliminated from sweeps. In most cases, selectivity persisted. These results support the idea of spectral delay lines that produce an overlap and summation of excitatory inputs only when a dynamic stimulus traverses a receptive field in one direction at a specific velocity.

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Neural Mechanisms Underlying Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Inferior Colliculus of the Pallid Bat

Journal of Neurophysiology ◽

10.1152/jn.00021.2006 ◽

2006 ◽

Vol 96 (3) ◽

pp. 1320-1336 ◽

Cited By ~ 46

Author(s):

Zoltan M. Fuzessery ◽

Marlin D. Richardson ◽

Michael S. Coburn

Keyword(s):

Inferior Colliculus ◽

High Frequency ◽

Tuning Curve ◽

Low Frequency ◽

Shape Selectivity ◽

Similar Rate ◽

Central Nucleus ◽

Arrival Times ◽

Sweep Direction ◽

Pallid Bat

This study describes mechanisms that underlie neuronal selectivity for the direction and rate of frequency-modulated sweeps in the central nucleus of the inferior colliculus (ICC) of the pallid bat ( Antrozous pallidus). This ICC contains a high percentage of neurons (66%) that respond selectively to the downward sweep direction of the bat's echolocation pulse. Some (19%) are specialists that respond only to downward sweeps. Most neurons (83%) are also tuned to sweep rates. A two-tone inhibition paradigm was used to describe inhibitory mechanisms that shape selectivity for sweep direction and rate. Two different mechanisms can create similar rate tuning. The first is an early on-best frequency inhibition that shapes duration tuning, which in turn determines rate tuning. In most neurons that are not duration tuned, a delayed high-frequency inhibition creates rate tuning. These neurons respond to fast sweep rates, but are inhibited as rate slows, and delayed inhibition overlaps excitation. In these neurons, starting a downward sweep within the excitatory tuning curve eliminates rate tuning. However, if rate tuning is shaped by duration tuning, this manipulation has no effect. Selectivity for the downward sweep direction is created by an early low-frequency inhibition that prevents responses to upward sweeps. In addition to this asymmetry in arrival times of low- and high-frequency inhibitions, the bandwidth of the low-frequency sideband was broader. Bandwidth influences the arrival time of inhibition during an FM sweep because a broader sideband will be encountered sooner. These findings show that similar spectrotemporal filters can be created by different mechanisms.

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Neural Mechanisms Underlying Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Auditory Cortex of the Pallid Bat

Journal of Neurophysiology ◽

10.1152/jn.00020.2006 ◽

2006 ◽

Vol 96 (3) ◽

pp. 1303-1319 ◽

Cited By ~ 69

Author(s):

Khaleel A. Razak ◽

Zoltan M. Fuzessery

Keyword(s):

Auditory Cortex ◽

High Frequency ◽

Cortical Neurons ◽

Arrival Time ◽

Narrow Band ◽

Low Frequency ◽

Sweep Rate ◽

Direction Selectivity ◽

Pallid Bats ◽

Pallid Bat

Frequency-modulated (FM) sweeps are common in vocalizations, including human speech. Selectivity for FM sweep rate and direction is present in the auditory cortex of many species. The present study sought to determine the mechanisms underlying FM sweep selectivity in the auditory cortex of pallid bats. In the pallid bat inferior colliculus (IC), two mechanisms underlie selectivity for FM sweep rate. The first mechanism depends on duration tuning for tones that arises as a consequence of early inhibition generated by an excitatory tone. The second mechanism depends on a narrow band of delayed high-frequency inhibition. Direction selectivity depends on a broad band of early low-frequency inhibition. Here, the contributions of these mechanisms to cortical FM sweep selectivity were determined in pentobarbital-anesthetized pallid bats. We show that the majority of cortical neurons tuned to echolocation frequencies are selective for the downward direction and rate of FM sweeps. Unlike in IC neurons tuned in the echolocation range, duration tuning is rare in cortical neurons with similar tuning. As in the IC, consistent spectrotemporal differences exist between low- and high-frequency sidebands. A narrow band of delayed high-frequency inhibition is necessary for FM rate selectivity. Low-frequency inhibition has a broad bandwidth, early arrival time, and creates direction selectivity. Cortical neurons respond better to slower FM rates and exhibit broader rate tuning than IC neurons. Relative arrival time of high-frequency inhibition is slower in the cortex than in the IC. Thus whereas similar mechanisms shape direction selectivity of neurons tuned in the echolocation range in the IC and the cortex, only one of the two mechanisms underlying rate selectivity in the IC is present in the cortex.

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Transient down-regulation of sound-induced c-Fos protein expression in the inferior colliculus after ablation of the auditory cortex

Frontiers in Neuroanatomy ◽

10.3389/fnana.2010.00141 ◽

2010 ◽

Vol 4 ◽

Cited By ~ 6

Author(s):

Cheryl Clarkson

Keyword(s):

Protein Expression ◽

Auditory Cortex ◽

Inferior Colliculus ◽

Down Regulation ◽

Fos Protein

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Disparity in interaural time difference improves the accuracy of neural representations of individual concurrent narrowband sounds in rat inferior colliculus and auditory cortex

Journal of Neurophysiology ◽

10.1152/jn.00284.2019 ◽

2020 ◽

Vol 123 (2) ◽

pp. 695-706

Author(s):

Lu Luo ◽

Na Xu ◽

Qian Wang ◽

Liang Li

Keyword(s):

Auditory Cortex ◽

Inferior Colliculus ◽

Interaural Time Difference ◽

Critical Role ◽

Low Frequency ◽

Time Difference ◽

Neural Representation ◽

Frequency Bands ◽

Neural Segregation ◽

Peripheral Auditory System

The central mechanisms underlying binaural unmasking for spectrally overlapping concurrent sounds, which are unresolved in the peripheral auditory system, remain largely unknown. In this study, frequency-following responses (FFRs) to two binaurally presented independent narrowband noises (NBNs) with overlapping spectra were recorded simultaneously in the inferior colliculus (IC) and auditory cortex (AC) in anesthetized rats. The results showed that for both IC FFRs and AC FFRs, introducing an interaural time difference (ITD) disparity between the two concurrent NBNs enhanced the representation fidelity, reflected by the increased coherence between the responses evoked by double-NBN stimulation and the responses evoked by single NBNs. The ITD disparity effect varied across frequency bands, being more marked for higher frequency bands in the IC and lower frequency bands in the AC. Moreover, the coherence between IC responses and AC responses was also enhanced by the ITD disparity, and the enhancement was most prominent for low-frequency bands and the IC and the AC on the same side. These results suggest a critical role of the ITD cue in the neural segregation of spectrotemporally overlapping sounds. NEW & NOTEWORTHY When two spectrally overlapped narrowband noises are presented at the same time with the same sound-pressure level, they mask each other. Introducing a disparity in interaural time difference between these two narrowband noises improves the accuracy of the neural representation of individual sounds in both the inferior colliculus and the auditory cortex. The lower frequency signal transformation from the inferior colliculus to the auditory cortex on the same side is also enhanced, showing the effect of binaural unmasking.

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Processing of spectral localization-informative changes in sound signals by neurons of inferior colliculus and auditory cortex of the house mouse Mus musculus

Journal of Evolutionary Biochemistry and Physiology ◽

10.1134/s0022093006050103 ◽

2006 ◽

Vol 42 (5) ◽

pp. 604-618

Author(s):

E. S. Malinina

Keyword(s):

Auditory Cortex ◽

Inferior Colliculus ◽

House Mouse ◽

Mus Musculus ◽

Spectral Localization

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Comparison of gain-like properties of eye position signals in inferior colliculus versus auditory cortex of primates

Frontiers in Integrative Neuroscience ◽

10.3389/fnint.2010.00121 ◽

2010 ◽

Cited By ~ 5

Author(s):

Maier

Keyword(s):

Auditory Cortex ◽

Inferior Colliculus ◽

Eye Position

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Sensitivity to binaural intensity and phase difference cues in kitten inferior colliculus

Journal of Neurophysiology ◽

10.1152/jn.1990.64.2.582 ◽

1990 ◽

Vol 64 (2) ◽

pp. 582-597 ◽

Cited By ~ 24

Author(s):

B. J. Blatchley ◽

J. F. Brugge

Keyword(s):

Auditory Cortex ◽

Inferior Colliculus ◽

Phase Difference ◽

Central Nucleus ◽

Intensity Difference ◽

Monotonic Functions ◽

Age Related ◽

Highly Correlated ◽

Intensity Functions ◽

Almost All

1. Responses of single neurons to monaural or binaural CF tones delivered through a closed and calibrated sound delivery system were studied in the central nucleus of the inferior colliculus (ICC) in ketamine and barbiturate-anesthetized kittens 4-105 days old. 2. Neurons from young kittens had elevated thresholds, some greater than 100 dB in the youngest kittens tested. Average thresholds in the ICC matched those previously measured in the auditory nerve (AN), cochlear nuclei (CN), and auditory cortex (CTX), suggesting that the drop in threshold as a function of age is primarily determined by development at the periphery. 3. Minimal first-spike latencies were relatively long in the youngest kittens, approaching adult values by the end of the third postnatal week. Latencies were distributed between values previously determined for the CN and auditory cortex and can be attributed to the centripetal development of the auditory system. 4. The range of frequencies that were effective in exciting ICC neurons was restricted in young kittens. Neurons having characteristic frequencies (CFs) greater than 7 kHz were not recorded before postnatal day 10. CF distribution matched that obtained in previous experiments from AN, CN, and CTX, reflecting the development of the cochlea. 5. Both monotonic and nonomonotonic spike count-versus-intensity functions were found in the youngest kittens. There was a tendency for monotonic functions from the youngest kittens to be steeper than those from older kittens. No age-related changes in the shapes of non-monotonic functions were found. 6. Sensitivity to interaural intensity difference (IID), tested by holding the intensity to the excitatory ear at a suprathreshold level and increasing the intensity of the stimulus to the inhibitory ear, was exhibited as early as 8 days after birth. The majority of the cells exhibiting sensitivity to IID (89.5%) were classified as EI cells, and almost all IID sensitive cells had CFs between 3 and 25 kHz. Within our sample the shapes of IID functions, as well as the operating range of the IID functions, closely resembled those obtained from the adult cat. Thresholds of excitation and of inhibition were highly correlated, suggesting that the ipsilateral and contralateral inputs to the ICC develop as a matched set. 7. Sensitivity to interaural phase difference (IPD), tested either by shifting the onset phase of a CF tone to one ear relative to the other or by presenting tones of slightly different frequency to the two ears, was present as early as 12 days after birth.(ABSTRACT TRUNCATED AT 400 WORDS)

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Responses in the Inferior Colliculus of the Guinea Pig to Concurrent Harmonic Series and the Effect of Inactivation of Descending Controls

Journal of Neurophysiology ◽

10.1152/jn.00451.2009 ◽

2010 ◽

Vol 103 (4) ◽

pp. 2050-2061 ◽

Cited By ~ 21

Author(s):

Kyle T. Nakamoto ◽

Trevor M. Shackleton ◽

Alan R. Palmer

Keyword(s):

Guinea Pig ◽

Auditory Cortex ◽

Inferior Colliculus ◽

Sound Level ◽

Harmonic Series ◽

Natural Environments ◽

Multiple Sources ◽

Spike Response ◽

Relative Level ◽

Communication Calls

One of the fundamental questions of auditory research is how sounds are segregated because, in natural environments, multiple sounds tend to occur at the same time. Concurrent sounds, such as two talkers, physically add together and arrive at the ear as a single input sound wave. The auditory system easily segregates this input into a coherent percept of each of the multiple sources. A common feature of speech and communication calls is their harmonic structure and in this report we used two harmonic complexes to study the role of the corticofugal pathway in the processing of concurrent sounds. We demonstrate that, in the inferior colliculus (IC) of the anesthetized guinea pig, deactivation of the auditory cortex altered the temporal and/or the spike response to the concurrent, monaural harmonic complexes. More specifically, deactivating the auditory cortex altered the representation of the relative level of the complexes. This suggests that the auditory cortex modulates the representation of the level of two harmonic complexes in the IC. Since sound level is a cue used in the segregation of auditory input, the corticofugal pathway may play a role in this segregation.

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