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

2017 ◽  
Vol 117 (4) ◽  
pp. 1636-1656 ◽  
Author(s):  
Roberto Valdizón-Rodríguez ◽  
Paul A. Faure
Keyword(s):  
Inferior Colliculus ◽  
Frequency Tuning ◽  
Stimulus Frequency ◽  
Onset Time ◽  
Extracellular Recording ◽  
Tone Frequency ◽  
Unit Recording ◽  
Synaptic Inputs ◽  
Big Brown Bat ◽  
Paired Tone

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 ( Eptesicus fuscus). 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. NEW & NOTEWORTHY 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.

scholarly journals Tuning for rate and duration of frequency-modulated sweeps in the mammalian inferior colliculus

2018 ◽  
Vol 120 (3) ◽  
pp. 985-997 ◽  
Author(s):  
James A. Morrison ◽  
Roberto Valdizón-Rodríguez ◽  
Daniel Goldreich ◽  
Paul A. Faure
Keyword(s):  
Inferior Colliculus ◽  
Bayesian Model ◽  
Model Comparison ◽  
Tuning Curve ◽  
Extracellular Recording ◽  
Sweep Rate ◽  
Center Frequency ◽  
Bayesian Model Comparison ◽  
Fm Signals ◽  
Big Brown Bat

Responses of auditory duration-tuned neurons (DTNs) are selective for stimulus duration. We used single-unit extracellular recording to investigate how the inferior colliculus (IC) encodes frequency-modulated (FM) sweeps in the big brown bat. It was unclear whether the responses of so-called “FM DTNs” encode signal duration, like classic pure-tone DTNs, or the FM sweep rate. Most FM cells had spiking responses selective for downward FM sweeps. We presented cells with linear FM sweeps whose center frequency (CEF) was set to the best excitatory frequency and whose bandwidth (BW) maximized the spike count. With these baseline parameters, we stimulated cells with linear FM sweeps randomly varied in duration to measure the range of excitatory FM durations and/or sweep rates. To separate FM rate and FM duration tuning, we doubled (and halved) the BW of the baseline FM stimulus while keeping the CEF constant and then recollected each cell’s FM duration tuning curve. If the cell was tuned to FM duration, then the best duration (or range of excitatory durations) should remain constant despite changes in signal BW; however, if the cell was tuned to the FM rate, then the best duration should covary with the same FM rate at each BW. A Bayesian model comparison revealed that the majority of neurons were tuned to the FM sweep rate, although a few cells showed tuning for FM duration. We conclude that the dominant parameter for temporal tuning of FM neurons in the IC is FM sweep rate and not FM duration. NEW & NOTEWORTHY Reports of inferior colliculus neurons with response selectivity to the duration of frequency-modulated (FM) stimuli exist, yet it remains unclear whether such cells are tuned to the FM duration or the FM sweep rate. To disambiguate these hypotheses, we presented neurons with variable-duration FM signals that were systematically manipulated in bandwidth. A Bayesian model comparison revealed that most temporally selective midbrain cells were tuned to the FM sweep rate and not the FM duration.

Responses to Social Vocalizations in the Inferior Colliculus of the Mustached Bat Are Influenced by Secondary Tuning Curves

2007 ◽  
Vol 98 (6) ◽  
pp. 3461-3472 ◽  
Author(s):  
Lars Holmstrom ◽  
Patrick D. Roberts ◽  
Christine V. Portfors
Keyword(s):  
Inferior Colliculus ◽  
Frequency Tuning ◽  
Tuning Curve ◽  
Extended Model ◽  
Complex Frequency ◽  
Neural Responses ◽  
Tone Frequency ◽  
Tuning Curves ◽  
Mustached Bat ◽  
Dual Functions

Neurons in the inferior colliculus (IC) of the mustached bat integrate input from multiple frequency bands in a complex fashion. These neurons are important for encoding the bat's echolocation and social vocalizations. The purpose of this study was to quantify the contribution of complex frequency interactions on the responses of IC neurons to social vocalizations. Neural responses to single tones, two-tone pairs, and social vocalizations were recorded in the IC of the mustached bat. Three types of data driven stimulus-response models were designed for each neuron from single tone and tone pair stimuli to predict the responses of individual neurons to social vocalizations. The first model was generated only using the neuron's primary frequency tuning curve, whereas the second model incorporated the entire hearing range of the animal. The extended model often predicted responses to many social vocalizations more accurately for multiply tuned neurons. One class of multiply tuned neuron that likely encodes echolocation information also responded to many of the social vocalizations, suggesting that some neurons in the mustached bat IC have dual functions. The third model included two-tone frequency tunings of the neurons. The responses to vocalizations were better predicted by the two-tone models when the neuron had inhibitory frequency tuning curves that were not near the neuron's primary tuning curve. Our results suggest that complex frequency interactions in the IC determine neural responses to social vocalizations and some neurons in IC have dual functions that encode both echolocation and social vocalization signals.

Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus

1996 ◽  
Vol 76 (2) ◽  
pp. 1059-1073 ◽  
Author(s):  
Z. M. Fuzessery ◽  
J. C. Hall
Keyword(s):  
Inferior Colliculus ◽  
Frequency Tuning ◽  
Response Magnitude ◽  
Central Nucleus ◽  
Gamma Aminobutyric Acid ◽  
Unit Recording ◽  
Tuning Curves ◽  
Sweep Direction ◽  
Species Specific

1. We examined the role of gamma-aminobutyric acid (GABA)-mediated inhibition in shaping excitatory tuning curves and creating selectivity for frequency-modulated (FM) sweeps in 29 neurons in the central nucleus of the inferior colliculus (ICC) of the pallid bat, with the use of single-unit recording coupled with the iontophoretic application of bicuculline methiodide (BIC), an antagonist of GABAA receptors. 2. BIC increased response magnitude 2 to 6 times over pretreatment levels in > 80% of neurons tested, and converted > 50% of nonmonotonic intensity-rate functions to monotonic or plateaued functions, demonstrating that GABAergic input normally limited response magnitude and inhibited responses at higher intensities. BIC typically had little effect on response thresholds, except in more specialized neurons that normally responded poorly to tones. In these cases, BIC disinhibited the neurons' responses to tones and lowered excitatory thresholds as much as 25 dB. 3. We examined the effects of BIC application on both excitatory and inhibitory tuning curves (measured with simultaneous 2-tone inhibition) to determine whether inhibitory curves were GABA mediated and whether removal of this inhibition was accompanied by an expansion of the excitatory curve. BIC had variable effects on the width of excitatory curves. In most cases, excitatory curves were at least slightly broadened, and expanded into regions previously occupied by inhibitory curves. In most cases, excitatory curves were at least slightly broadened, and expanded into regions previously occupied by inhibitory curves. However, in a few cases, inhibitory curves could be eliminated without an expansion of the excitatory curve. The greatest effect was seen in neurons with closed excitatory tuning curves; blocking GABAergic input caused the curves to open, allowing the neurons to respond at higher intensities. 4. Approximately 50% of the neurons in the ICC tuned to the spectrum of the bat's downward FM sweeping biosonar pulse respond preferentially to downward FM sweeps and not to upward sweeps, tones, or noise. In all neurons tested, BIC at least partially destroyed selectivity for sweep direction. This destruction could occur, however, without a loss of response exclusivity; in some cases, the neurons still did not respond to tones or noise. These results suggest that response selectivity for a species-specific signal is created by GABAergic input to ICC neurons. These results are used to suggest a mechanism that creates selectivity for FM sweep direction.

scholarly journals Effect of sound pressure level on contralateral inhibition underlying duration-tuned neurons in the mammalian inferior colliculus

2019 ◽  
Vol 122 (1) ◽  
pp. 184-202
Author(s):  
Roberto Valdizón-Rodríguez ◽  
Dominika Kovaleva ◽  
Paul A. Faure
Keyword(s):  
Inferior Colliculus ◽  
Sound Pressure Level ◽  
Time Course ◽  
Sound Pressure ◽  
Dynamic Range ◽  
Onset Time ◽  
Pressure Level ◽  
Half Maximum ◽  
Synaptic Inputs ◽  
Rate Level

Duration tuning in the mammalian inferior colliculus (IC) is created by the interaction of excitatory and inhibitory synaptic inputs. We used extracellular recordings and paired tone stimulation to measure the strength and time course of the contralateral inhibition underlying duration-tuned neurons (DTNs) in the IC of the awake bat. The onset time of a short, best duration (BD), excitatory probe tone set to +10 dB (re threshold) was varied relative to the onset of a longer-duration, nonexcitatory (NE) suppressor tone whose sound pressure level (SPL) was varied. Spikes evoked by the roving BD tone were suppressed when the stationary NE tone amplitude was at or above the BD tone threshold. When the NE tone was increased from 0 to +10 dB, the inhibitory latency became shorter than the excitatory first-spike latency and the duration of inhibition increased, but no further changes occurred at +20 dB (re BD tone threshold). We used the effective duration of inhibition as a function of the NE tone amplitude to obtain suppression-level functions that were used to estimate the inhibitory half-maximum SPL (ISPL50). We also measured rate-level functions of DTNs with single BD tones varied in SPL and modeled the excitatory half-maximum SPL (ESPL50). There was a correlation between the ESPL50 and ISPL50, and the dynamic range of excitation and inhibition were similar. We conclude that the strength of inhibition changes in proportion to excitation as a function of SPL, and this feature likely contributes to the amplitude tolerance of the responses of DTNs. NEW & NOTEWORTHY Duration-tuned neurons arise from excitatory and inhibitory synaptic inputs offset in time. We measured the strength and time course of inhibition to changes in sound level. The onset of inhibition shortened while its duration lengthened as the stimulus level increased from 0 to +10 dB re threshold; however, no further changes were observed at +20 dB. Excitatory rate-level and inhibitory suppression-level response functions were strongly correlated, suggesting a mechanism for level tolerance in duration tuning.

Neural Tuning to Sound Duration in the Inferior Colliculus of the Big Brown Bat, Eptesicus fuscus

1997 ◽  
Vol 77 (5) ◽  
pp. 2360-2372 ◽  
Author(s):  
Daphna Ehrlich ◽  
John H. Casseday ◽  
Ellen Covey
Keyword(s):  
Inferior Colliculus ◽  
Stimulus Duration ◽  
Frequency Tuning ◽  
Temporal Structure ◽  
Eptesicus Fuscus ◽  
Broadband Noise ◽  
Inhibitory Input ◽  
Echolocation Calls ◽  
Big Brown Bat ◽  
Sound Duration

Ehrlich, Daphna, John H. Casseday, and Ellen Covey. Neural tuning to sound duration in the inferior colliculus of the big brown bat, Eptesicus fuscus. J. Neurophysiol. 77: 2360–2372, 1997. Neural tuning to different sound durations may be a useful filter for identification of certain sounds, especially those that are biologically important. The auditory midbrains of mammals and amphibians contain neurons that appear to be tuned to sound duration. In amphibians, neurons are tuned to durations of sound that are biologically important. The purpose of this study was to characterize responses of neurons in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus, to sounds of different durations. Our aims were to determine what percent of neurons are duration tuned and how best durations are correlated to durations of echolocation calls, and to examine response properties that may be relevant to the mechanism for duration tuning, such as latency and temporal firing pattern; we also examined frequency tuning and rate-level functions. We recorded from 136 single units in the central nucleus of the IC of unanesthetized bats. The stimuli were pure tones, frequency-modulated sweeps, and broadband noise. The criterion for duration tuning was an increase in spike count of ≥50% at some durations compared with others. Of the total units sampled, 36% were tuned to stimulus duration. All of these units were located in the caudal half of the IC. Best duration for most units ranged from <1 to 10 ms, but a few had best durations up to ≥20 ms. This range is similar to the range of durations of echolocation calls used by Eptesicus. All duration-tuned neurons responded transiently. The minimum latency was always longer than the best duration. Duration-tuned units have best durations and best frequencies that match the temporal structure and frequency range of the echolocation calls. Thus the results raise the hypothesis that neurons in the IC of Eptesicus, and probably the auditory midbrain of other vertebrates, are tuned to biologically important sound durations. We suggest a model for duration tuning consisting of three components: 1) inhibitory input that is correlated with the onset of the stimulus and is sustained for the stimulus duration; 2) transient excitation that is correlated with the offset of the stimulus; and 3) transient excitation that is correlated with the onset of the stimulus but is delayed in time relative to the onset of inhibition. For the neuron to fire, the two excitatory events must coincide in time; noncoincident excitatory events are not sufficient.

scholarly journals Tone-Specific and Nonspecific Plasticity of Inferior Colliculus Elicited by Pseudo-Conditioning: Role of Acetylcholine and Auditory and Somatosensory Cortices

2009 ◽  
Vol 102 (2) ◽  
pp. 941-952 ◽  
Author(s):  
Weiqing Ji ◽  
Nobuo Suga
Keyword(s):  
Inferior Colliculus ◽  
Frequency Tuning ◽  
Muscarinic Acetylcholine Receptor ◽  
Somatosensory Cortices ◽  
Big Brown Bat ◽  
Auditory Response ◽  
Response Increase ◽  
Plastic Changes ◽  
Central Auditory Neurons

Experience-dependent plasticity in the central sensory systems depends on activation of both the sensory and neuromodulatory systems. Sensitization or nonspecific augmentation of central auditory neurons elicited by pseudo-conditioning with unpaired conditioning tonal (CS) and unconditioned electric leg (US) stimuli is quite different from tone-specific plasticity, called best frequency (BF) shifts, of the neurons elicited by auditory fear conditioning with paired CS and US. Therefore the neural circuits eliciting the nonspecific augmentation must be different from that eliciting the BF shifts. We first examined plastic changes in the response properties of collicular neurons of the big brown bat elicited by pseudo-conditioning and found that it elicited prominent nonspecific augmentation—an auditory response increase, a frequency-tuning broadening, and a threshold decreas—and that, in addition, it elicited a small short-lasting BF shift only when the CS frequency was 5 kHz lower than the BF of a recorded neuron. We examined the role of acetylcholine and the auditory and somatosensory cortices in these collicular changes. The development of the nonspecific augmentation was affected little by a muscarinic acetylcholine receptor antagonist applied to the inferior colliculus and by a GABAA receptor agonist applied to the auditory or somatosensory cortex. However, these drugs abolished the small short-lasting BF shift as they abolished the large long-lasting cortical and short-lasting collicular BF shifts elicited by the conditioning. These results indicate that, different from the BF shift, the nonspecific augmentation of the inferior colliculus depends on neither the cholinergic neuromodulator nor the auditory and somatosensory cortices.

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

2014 ◽  
Vol 111 (10) ◽  
pp. 2047-2060 ◽  
Author(s):  
James A. Morrison ◽  
Faranak Farzan ◽  
Thane Fremouw ◽  
Riziq Sayegh ◽  
Ellen Covey ◽  
...  
Keyword(s):  
Inferior Colliculus ◽  
Spatial Organization ◽  
Frequency Tuning ◽  
Stimulus Frequency ◽  
Neural Mechanism ◽  
Auditory Pathway ◽  
Complex Signal ◽  
Trade Off ◽  
Tuning Curves ◽  
Engineering Theory

Neurons throughout the mammalian central auditory pathway respond selectively to stimulus frequency and amplitude, and some are also selective for stimulus duration. First found in the auditory midbrain or inferior colliculus (IC), these duration-tuned neurons (DTNs) provide a potential neural mechanism for encoding temporal features of sound. In this study, we investigated how having an additional neural response filter, one selective to the duration of an auditory stimulus, influences frequency tuning and neural organization by recording single-unit responses and measuring the dorsal-ventral position and spectral-temporal tuning properties of auditory DTNs from the IC of the awake big brown bat ( Eptesicus fuscus). Like other IC neurons, DTNs were tonotopically organized and had either V-shaped, U-shaped, or O-shaped frequency tuning curves (excitatory frequency response areas). We hypothesized there would be an interaction between frequency and duration tuning in DTNs, as electrical engineering theory for resonant filters dictates a trade-off in spectral-temporal resolution: sharp tuning in the frequency domain results in poorer resolution in the time domain and vice versa. While the IC is a more complex signal analyzer than an electrical filter, a similar operational trade-off could exist in the responses of DTNs. Our data revealed two patterns of spectro-temporal sensitivity and spatial organization within the IC: DTNs with sharp frequency tuning and broad duration tuning were located in the dorsal IC, whereas cells with wide spectral tuning and narrow temporal tuning were found in the ventral IC.

Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms

1988 ◽  
Vol 60 (6) ◽  
pp. 1799-1822 ◽  
Author(s):  
G. Langner ◽  
C. E. Schreiner
Keyword(s):  
Firing Rate ◽  
Inferior Colliculus ◽  
Amplitude Modulation ◽  
Transfer Functions ◽  
Modulation Frequency ◽  
Temporal Structure ◽  
Stimulus Frequency ◽  
Single Units ◽  
Central Nucleus ◽  
Multiple Unit

1. Temporal properties of single- and multiple-unit responses were investigated in the inferior colliculus (IC) of the barbiturate-anesthetized cat. Approximately 95% of recording sites were located in the central nucleus of the inferior colliculus (ICC). Responses to contralateral stimulation with tone bursts and amplitude-modulated tones (100% sinusoidal modulation) were recorded. Five response parameters were determined for neurons at each location: 1) characteristic frequency (CF); 2) onset latency of responses to CF-tones 60 dB above threshold; 3) Q10 dB (CF divided by bandwidth of tuning curve 10 dB above threshold); 4) best modulation frequency for firing rate (rBMF or BMF; amplitude modulation frequency that elicited the highest firing rate); and 5) best modulation frequency for synchronization (sBMF; amplitude modulation frequency that elicited the highest degree of phase-locking to the modulation frequency). 2. Response characteristics for single units and multiple units corresponded closely. A BMF was obtained at almost all recording sites. For units with a similar CF, a range of BMFs was observed. The upper limit of BMF increased approximately proportional to CF/4 up to BMFs as high as 1 kHz. The lower limit of encountered BMFs for a given CF also increased slightly with CF. BMF ranges for single-unit and multiple-unit responses were similar. Twenty-three percent of the responses revealed rBMFs between 10 and 30 Hz, 51% between 30 and 100 Hz, 18% between 100 and 300 Hz, and 8% between 300 and 1000 Hz. 3. For single units with modulation transfer functions of bandpass characteristics, BMFs determined for firing rate and synchronization were similar (r2 = 0.95). 4. Onset latencies for responses to CF tones 60 dB above threshold varied between 4 and 120 ms. Ninety percent of the onset latencies were between 5 and 18 ms. A range of onset latencies was recorded for different neurons with any given CF. The onset response latency of a given unit or unit cluster was significantly correlated with the period of the BMF and the period of the CF (P less than 0.05). 5."Intrinsic oscillations" of short duration, i.e., regularly timed discharges of units in response to stimuli without a corresponding temporal structure, were frequently observed in the ICC. Oscillation intervals were commonly found to be integer multiples of 0.4 ms. Changes of stimulus frequency or intensity had only minor influences on these intrinsic oscillations.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Tonotopic and non-auditory organization of the mouse dorsal inferior colliculus revealed by two-photon imaging

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Aaron Benson Wong ◽  
J Gerard G Borst
Keyword(s):  
Inferior Colliculus ◽  
Spatial Organization ◽  
Functional Organization ◽  
Frequency Tuning ◽  
Gabaergic Neurons ◽  
Two Photon ◽  
Spontaneous Movements ◽  
Multimodal Information ◽  
Auditory Organization

The dorsal (DCIC) and lateral cortices (LCIC) of the inferior colliculus are major targets of the auditory and non-auditory cortical areas, suggesting a role in complex multimodal information processing. However, relatively little is known about their functional organization. We utilized in vivo two-photon Ca2+ imaging in awake mice expressing GCaMP6s in GABAergic or non-GABAergic neurons in the IC to investigate their spatial organization. We found different classes of temporal responses, which we confirmed with simultaneous juxtacellular electrophysiology. Both GABAergic and non-GABAergic neurons showed spatial microheterogeneity in their temporal responses. In contrast, a robust, double rostromedial-caudolateral gradient of frequency tuning was conserved between the two groups, and even among the subclasses. This, together with the existence of a subset of neurons sensitive to spontaneous movements, provides functional evidence for redefining the border between DCIC and LCIC.

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