Responses to pure tones and linear FM components of the CF ? FM biosonar signal by single units in the inferior colliculus of the mustached bat

O’Neill, William E.

doi:10.1007/bf01350077

Cited by 60 publications

(32 citation statements)

References 45 publications

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“…Compared with other species of FM bats, which have Ͻ15% of neurons that are selective for the echolocation pulse (O'Neill 1985;Suga 1965b), nearly 70% of neurons tuned between 30 and 60 kHz in the pallid bat IC and cortex (Fuzessery 1994;Razak and Fuzessery 2002;this study;Fuzessery et al, unpublished observation) show such selectivity. As suggested before, one reason the pallid bat FM selective region is so specialized may be the gleaning lifestyle of the pallid bat (Fuzessery 1994).…”

Section: Strong Selectivity For Behaviorally Relevant Sounds In the Pmentioning

confidence: 74%

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

Razak

Fuzessery

2006

Journal of Neurophysiology

140

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Razak, Khaleel A. and Zoltan M. Fuzessery. Neural mechanisms underlying selectivity for the rate and direction of frequencymodulated sweeps in the auditory cortex of the pallid bat. J Neurophysiol 96: 1303-1319, 2006. First published June 14, 2006 doi:10.1152/jn.00020.2006 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. I N T R O D U C T I O NSelectivity for the rate and direction of stimulus movement across the receptor surface is a common feature of sensory systems. Although neural selectivity for these attributes plays an important role in representing motion in vision (Newsome et al. 1985) and frequency modulations in audition (Suga 1965a), the mechanisms underlying selectivity are topics of debate. In visual and somatosensory cortices, facilitation within the receptive field and inhibition from the receptive field surround are two mechanisms proposed to underlie direction selectivity (Gardner and Costanzo 1980;Movshon et al. 1978;Murthy and Humphrey 1999). In the visual cortex, rate (velocity) selectivity may arise either through sideband inhibition (Goodwin and Henry 1978), facilitation within the receptive field (RF; Duysens et al. 1985a), or through temporal properties such as duration tuning (Duysens et al. 1985b). These similarities suggest that rate and direction selectivity arise through comm...

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Section: Strong Selectivity For Behaviorally Relevant Sounds In the Pmentioning

confidence: 74%

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

Razak

Fuzessery

2006

Journal of Neurophysiology

140

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“…This methodology selected for cells that responded to both tones and FM sweeps, and thereby may have missed "FM specialized" units that respond to FM sweeps but not to tones. While FM specialized units are relatively common in the IC of some species of bats, such units comprise less than 2% of ICC and ICXv units in the mustached bat (O'Neill, 1985;Gordon and O'Neill, 2000). Once preliminary measures were obtained, we tested the unit using an FM stimulus set followed by presentation of a two-tone stimulus set for constructing the conditioned response area.…”

Section: Methodsmentioning

confidence: 99%

“…Bats were housed in a temperature (24°C ) and relative humidity (80%) controlled flight room and fed fortified mealworms. Surgery to mount a head-restraining post, implant an indifferent electrode, and expose the IC was performed under methoxyflurane anesthesia (Metofane, Pittman-Moore) using techniques described previously (O'Neill, 1985). For the experiments, awake bats were administered a low dose of an opioid agonist (butorphanol tartrate, 0.7 mg/kg i.p.…”

Section: Preparationmentioning

confidence: 99%

On the prediction of sweep rate and directional selectivity for FM sounds from two-tone interactions in the inferior colliculus

Brimijoin

O’Neill

2005

Hearing Research

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Two-tone stimuli have traditionally been used to reveal regions of inhibition in auditory spectral receptive fields, particularly for neurons with low spontaneous rates. These techniques reveal how different frequencies excite or suppress the response to an excitatory frequency of a cell, but have often been assessed at a fixed masker-probe time interval. We used a variation of this methodology determine whether two-tone spectrotemporal interactions can account for ratedependent directional selectivity for frequency modulations (FM) in the mustached bat inferior colliculus (IC). First, we quantified the response to upward and downward sweeping, linear, fixedbandwidth FM tones centered at a unit's characteristic frequency (CF) at 6 sweep durations ranging from 2 to 64 ms. Then, to examine how responses to instantaneous frequencies contained within the sweeps might interact in time, we varied the frequency and relative onset of a brief (4 ms) "conditioner" tone paired with a fixed 4-ms CF probe tone. We constructed "conditioned response areas" (CRA) depicting regions of suppression and facilitation of the probe tone caused by the conditioning tone. We classified the CRAs as predominantly excitatory (40.9%), inhibitory (22.7%), or mixed (36.4%). To generate FM response predictions, the CRAs were multiplied with spectrograms of the same sweeps used to assess response to FM. The predictions of FM rate and directionality were accurate by our criteria in approximately 20% of units. Conversely, the CRAs from the remaining units failed to predict FM responses as accurately, suggesting that most IC units respond differently to FM sweeps than they do to tone-pairs matched to the instantaneous frequencies contained in those sweeps. The implications of these results for models of FM directionality are discussed.

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“…Such neurons are common throughout the mustached bat IC (Leroy and Wenstrup 2000;Mittmann and Wenstrup 1995;Nataraj and Wenstrup 2006;O'Neill 1985;Portfors and Wenstrup 1999) and occur in other species and auditory centers (Imig et al 1997;Kadia and Wang 2003;Portfors and Felix 2005;Rauschecker et al 1995;Sutter et al 1999).…”

Section: Combination-sensitive Inhibitory Interactions Arise Below Anmentioning

confidence: 99%

“…A second class of combination-sensitive neurons (Mittmann and Wenstrup 1995;O'Neill 1985), showing inhibitory interactions between spectral elements (Fig. 1B), may originate below the IC.…”

mentioning

confidence: 99%

Intracellular Recordings From Combination-Sensitive Neurons in the Inferior Colliculus

Peterson

Voytenko²,

Gans³

et al. 2008

Journal of Neurophysiology

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Peterson DC, Voytenko S, Gans D, Galazyuk A, Wenstrup J. Intracellular recordings from combination-sensitive neurons in the inferior colliculus. J Neurophysiol 100: 629-645, 2008. First published May 21, 2008 doi:10.1152/jn.90390.2008. In vertebrate auditory systems, specialized combination-sensitive neurons analyze complex vocal signals by integrating information across multiple frequency bands. We studied combinationsensitive interactions in neurons of the inferior colliculus (IC) of awake mustached bats, using intracellular somatic recording with sharp electrodes. Facilitated combinatorial neurons are coincidence detectors, showing maximum facilitation when excitation from low-and high-frequency stimuli coincide. Previous work showed that facilitatory interactions originate in the IC, require both low and high frequency-tuned glycinergic inputs, and are independent of glutamatergic inputs. These results suggest that glycinergic inputs evoke facilitation through either postinhibitory rebound or direct depolarizing mechanisms. However, in 35 of 36 facilitated neurons, we observed no evidence of low frequency-evoked transient hyperpolarization or depolarization that was closely related to response facilitation. Furthermore, we observed no evidence of shunting inhibition that might conceal inhibitory inputs. Since these facilitatory interactions originate in IC neurons, the results suggest that inputs underlying facilitation are electrically segregated from the soma. We also recorded inhibitory combinatorial interactions, in which low frequency sounds suppress responses to higher frequency signals. In 43% of 118 neurons, we observed low frequency-evoked hyperpolarizations associated with combinatorial inhibition. For these neurons, we conclude that low frequency-tuned inhibitory inputs terminate on neurons primarily excited by high-frequency signals; these inhibitory inputs may create or enhance inhibitory combinatorial interactions. In the remainder of inhibited combinatorial neurons (57%), we observed no evidence of low frequency-evoked hyperpolarizations, consistent with observations that inhibitory combinatorial responses may originate in lateral lemniscal nuclei.

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Responses to pure tones and linear FM components of the CF ? FM biosonar signal by single units in the inferior colliculus of the mustached bat

Cited by 60 publications

References 45 publications

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

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

On the prediction of sweep rate and directional selectivity for FM sounds from two-tone interactions in the inferior colliculus

Intracellular Recordings From Combination-Sensitive Neurons in the Inferior Colliculus

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