Organization and trade-off of spectro-temporal tuning properties of duration-tuned neurons in the mammalian inferior colliculus

Morrison, J. A.; Farzan, Faranak; Fremouw, Thane; Sayegh, Riziq; Covey, Ellen; Faure, Paul

doi:10.1152/jn.00850.2013

Cited by 10 publications

(14 citation statements)

References 87 publications

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“…5A; R 2 ϭ 0.639, P Ͻ Ͻ 0.001). This finding demonstrates that DTNs are also tonotopically organized, thus replicating previous findings about duration tuning in the IC (Haplea et al 1994;Jen and Wu 2006;Morrison et al 2014;Pinheiro et al 1991;Sayegh et al 2012). Most of the DTNs in our sample (97.6%) had BEFs that fell between 20 and 70 kHz.…”

Section: Tonotopic Organization Of Dtns In Icsupporting

confidence: 91%

“…The spectral tuning of auditory DTNs is of particular interest given that spectral and temporal features of biological sounds are often comodulated (Heil et al 1992;Suga 1984). Recent studies have shown that DTNs in the mammalian inferior colliculus (IC) show a trade-off in their spectro-temporal response resolutions in a manner analogous to resonant electrical filters (Morrison et al 2014). Moreover, the frequency selectivity of a DTN can change when it is stimulated with sound pulses that are varied in duration (Wu and Jen 2008a).…”

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confidence: 99%

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Frequency tuning of synaptic inhibition underlying duration-tuned neurons in the mammalian inferior colliculus

Valdizón-Rodríguez

Faure

2017

Journal of Neurophysiology

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Inhibition plays an important role in creating the temporal response properties of duration-tuned neurons (DTNs) in the mammalian inferior colliculus (IC). Neurophysiological and computational studies indicate that duration selectivity in the IC is created through the convergence of excitatory and inhibitory synaptic inputs offset in time. We used paired-tone stimulation and extracellular recording to measure the frequency tuning of the inhibition acting on DTNs in the IC of the big brown bat (). We stimulated DTNs with pairs of tones differing in duration, onset time, and frequency. The onset time of a short, best-duration (BD), probe tone set to the best excitatory frequency (BEF) was varied relative to the onset of a longer-duration, nonexcitatory (NE) tone whose frequency was varied. When the NE tone frequency was near or within the cell's excitatory bandwidth (eBW), BD tone-evoked spikes were suppressed by an onset-evoked inhibition. The onset of the spike suppression was independent of stimulus frequency, but both the offset and duration of the suppression decreased as the NE tone frequency departed from the BEF. We measured the inhibitory frequency response area, best inhibitory frequency (BIF), and inhibitory bandwidth (iBW) of each cell. We found that the BIF closely matched the BEF, but the iBW was broader and usually overlapped the eBW measured from the same cell. These data suggest that temporal selectivity of midbrain DTNs is created and preserved by having cells receive an onset-evoked, constant-latency, broadband inhibition that largely overlaps the cell's excitatory receptive field. We conclude by discussing possible neural sources of the inhibition. Duration-tuned neurons (DTNs) arise from temporally offset excitatory and inhibitory synaptic inputs. We used single-unit recording and paired-tone stimulation to measure the spectral tuning of the inhibitory inputs to DTNs. The onset of inhibition was independent of stimulus frequency; the offset and duration of inhibition systematically decreased as the stimulus departed from the cell's best excitatory frequency. Best inhibitory frequencies matched best excitatory frequencies; however, inhibitory bandwidths were more broadly tuned than excitatory bandwidths.

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Section: Tonotopic Organization Of Dtns In Icsupporting

confidence: 91%

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confidence: 99%

Frequency tuning of synaptic inhibition underlying duration-tuned neurons in the mammalian inferior colliculus

Valdizón-Rodríguez

Faure

2017

Journal of Neurophysiology

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“…This result is also consistent with the finding that some DTNs are sensitive to binaural interaural level difference and interaural time difference cues important for sound localization ). Furthermore, a study on the interaction between frequency and duration tuning demonstrated that DTNs exhibited two patterns of spectro-temporal sensitivity and spatial organization within the IC: cells with sharp frequency tuning and broad duration tuning were located in the dorsal IC, and cells with wide spectral tuning and narrow temporal tuning were located in the ventral IC (Morrison et al 2014). Bats systematically vary the duration of their echolocation calls while foraging, and there are a number of reasons why it would be helpful for the bat to "know" when an external signal of a specific frequency (or bandwidth), amplitude (intensity), and duration was received by each ear.…”

Section: Discussionmentioning

confidence: 99%

“…In our dataset DTNs varied in their response characteristics from having very narrow (responding to only 1 or 2 durations) to quite broad (responding to a wide range of durations) temporal tuning curves (see also Morrison et al 2014). Therefore, the perfor-mance of a decoder using randomly selected DTNs as inputs would be highly dependent on the particular subset of cells chosen.…”

Section: Decoding Stimulus Durationmentioning

confidence: 99%

Decoding stimulus duration from neural responses in the auditory midbrain

Aubie

Sayegh

Fremouw

et al. 2014

Journal of Neurophysiology

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(DTNs). Temporal specificity in their spiking suggests that one function of DTNs is to encode stimulus duration; however, the efficacy of duration encoding by DTNs has yet to be investigated. Herein, we characterize the information content of individual cells and a population of DTNs from the mammalian inferior colliculus (IC) by measuring the stimulus-specific information (SSI) and estimated Fisher information (FI) of spike count responses. We found that SSI was typically greatest for those stimulus durations that evoked maximum spike counts, defined as best duration (BD) stimuli, and that FI was maximal for stimulus durations off BD where sensitivity to a change in duration was greatest. Using population data, we demonstrate that a maximum likelihood estimator (MLE) can accurately decode stimulus duration from evoked spike counts. We also simulated a two-alternative forced choice task by having MLE models decide whether two durations were the same or different. With this task we measured the just-noticeable difference threshold for stimulus duration and calculated the corresponding Weber fractions across the stimulus domain. Altogether, these results demonstrate that the spiking responses of DTNs from the mammalian IC contain sufficient information for the CNS to encode, decode, and discriminate behaviorally relevant auditory signal durations. big brown bat; Eptesicus fuscus; Fisher information, inferior colliculus; just-noticeable difference; stimulus-specific information, temporal processing; Weber fraction DURATION-TUNED NEURONS (DTNs) are ideal candidates for encoding spectral, intensity, and temporal information about an auditory stimulus because they respond selectively to the frequency, amplitude, and duration of acoustic signals. First reported in the torus semicircularis of frogs and subsequently the inferior colliculus (IC) of bats, DTNs have now been recorded from the auditory midbrain, thalamus, and cortex in a variety of vertebrates, and from the mammalian visual cortex (see Sayegh et al. 2011, for review). To date, the electrophysiological properties and underlying synaptic inputs responsible for creating the temporally selective responses of DTNs have been a major research focus, but a quantitative analysis of the information content and encoding efficiency of any neural system is important for linking neurophysiology to behavior and perception because it can suggest limits on the efficacy of information representation. Information theoretic measurements have previously been used to characterize the spiking responses of visual (Strong et al. 1998;Tolhurst et al. 2009 Sensory neurons in general, and auditory neurons in particular, are often viewed as feature detectors that have a preferred value in stimulus domains such as frequency or amplitude, and they encode the domain with spike counts (or rates) and latencies that vary as a function of the stimulus. We measured spike counts and latencies from auditory DTNs in the mammalian IC to characterize the information content of duration-selective ne...

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“…Detailed explanations of animal care and institutional approval, surgical preparation and anaesthesia, stimulus generation, and neural recording procedures have been published [21,22].…”

Section: Methodsmentioning

confidence: 99%

Testing inferior colliculus neurons for selectivity to the rate or duration of frequency modulated sweeps

Faure¹,

Morrison²,

Valdizón-Rodríguez³

2018

AIP Conference Proceedings

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Abstract.Here we propose a method for testing how the responses of so-called "FM duration-tuned neurons (DTNs)" encode temporal properties of frequency modulated (FM) sweeps to determine if the responses of so-called "FM duration-tuned neurons (DTNs)" are tuned to FM rate or FM duration. Based on previous studies it was unclear if the responses of "FM DTNs" were tuned to signal duration, like pure-tone DTNs, or FM sweep rate. We tested this using single-unit extracellular recording in the inferior colliculus (IC) of the big brown bat (Eptesicus fuscus). We presented IC cells with linear FM sweeps that were varied in FM center frequency (CEF) and spectral bandwidth (BW) to measure the FM rate tuning responses of a cell. We also varied FM signal duration to measure the best duration (BD) and temporal BW of duration tuning of a cell. We then doubled (and halved) the best FM BW, while keeping the CEF constant, and remeasured the BD and temporal BW of duration tuning with FM bandwidth manipulated signals. We reasoned that the range of excitatory signal durations should not change in a true FM DTN whose responses are tuned to signal duration; however, when stimulated with bandwidth manipulated FM sounds the range of excitatory signal durations should predictably vary in a FM rate-tuned cell. Preliminary data indicate that our stimulus paradigm can disambiguate whether the evoked responses of an IC neuron are FM sweep rate tuned or FM duration tuned.

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Organization and trade-off of spectro-temporal tuning properties of duration-tuned neurons in the mammalian inferior colliculus

Cited by 10 publications

References 87 publications

Frequency tuning of synaptic inhibition underlying duration-tuned neurons in the mammalian inferior colliculus

Frequency tuning of synaptic inhibition underlying duration-tuned neurons in the mammalian inferior colliculus

Decoding stimulus duration from neural responses in the auditory midbrain

Testing inferior colliculus neurons for selectivity to the rate or duration of frequency modulated sweeps

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