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PLoS Biology Jun 2019Accurately resolving frequency components in sounds is essential for sound recognition, yet there is little direct evidence for how frequency selectivity is preserved or...
Accurately resolving frequency components in sounds is essential for sound recognition, yet there is little direct evidence for how frequency selectivity is preserved or newly created across auditory structures. We demonstrate that prepotentials (PPs) with physiological properties resembling presynaptic potentials from broadly tuned brainstem inputs can be recorded concurrently with postsynaptic action potentials in inferior colliculus (IC). These putative brainstem inputs (PBIs) are broadly tuned and exhibit delayed and spectrally interleaved excitation and inhibition not present in the simultaneously recorded IC neurons (ICNs). A sharpening of tuning is accomplished locally at the expense of spike-timing precision through nonlinear temporal integration of broadband inputs. A neuron model replicates the finding and demonstrates that temporal integration alone can degrade timing precision while enhancing frequency tuning through interference of spectrally in- and out-of-phase inputs. These findings suggest that, in contrast to current models that require local inhibition, frequency selectivity can be sharpened through temporal integration, thus supporting an alternative computational strategy to quickly refine frequency selectivity.
Topics: Acoustic Stimulation; Action Potentials; Animals; Auditory Pathways; Auditory Perception; Cats; Electrophysiological Phenomena; Inferior Colliculi; Neural Inhibition; Neurons; Sound; Synaptic Potentials
PubMed: 31233489
DOI: 10.1371/journal.pbio.2005861 -
Journal of Neurophysiology Jul 2015The century-old duplex theory of sound localization posits that low- and high-frequency sounds are localized with two different acoustical cues, interaural time and...
The century-old duplex theory of sound localization posits that low- and high-frequency sounds are localized with two different acoustical cues, interaural time and level differences (ITDs and ILDs), respectively. While behavioral studies in humans and behavioral and neurophysiological studies in a variety of animal models have largely supported the duplex theory, behavioral sensitivity to ILD is curiously invariant across the audible spectrum. Here we demonstrate that auditory midbrain neurons in the chinchilla (Chinchilla lanigera) also encode ILDs in a frequency-invariant manner, efficiently representing the full range of acoustical ILDs experienced as a joint function of sound source frequency, azimuth, and distance. We further show, using Fisher information, that nominal "low-frequency" and "high-frequency" ILD-sensitive neural populations can discriminate ILD with similar acuity, yielding neural ILD discrimination thresholds for near-midline sources comparable to behavioral discrimination thresholds estimated for chinchillas. These findings thus suggest a revision to the duplex theory and reinforce ecological and efficiency principles that hold that neural systems have evolved to encode the spectrum of biologically relevant sensory signals to which they are naturally exposed.
Topics: Acoustic Stimulation; Acoustics; Action Potentials; Animals; Auditory Pathways; Chinchilla; Cues; Female; Inferior Colliculi; Information Theory; Male; Microelectrodes; Neurons; Sound Localization
PubMed: 25972580
DOI: 10.1152/jn.00062.2015 -
The Journal of Comparative Neurology Feb 2022Sound localization critically relies on brainstem neurons that compare information from the two ears. The conventional role of the lateral superior olive (LSO) is...
Sound localization critically relies on brainstem neurons that compare information from the two ears. The conventional role of the lateral superior olive (LSO) is extraction of intensity differences; however, it is increasingly clear that relative timing, especially of transients, is also an important function. Cellular diversity within the LSO that is not well understood may underlie its multiple roles. There are glycinergic inhibitory and glutamatergic excitatory principal neurons in the LSO, however, there is some disagreement regarding their relative distribution and projection pattern. Here we employ in situ hybridization to definitively identify transmitter types combined with retrograde labeling of projections to the inferior colliculus (IC) to address these questions. Excitatory LSO neurons were more numerous (76%) than inhibitory ones. A smaller proportion of inhibitory neurons were IC-projecting (45% vs. 64% for excitatory) suggesting that inhibitory LSO neurons may have more projections to other regions such the lateral lemniscus or more distributed IC projections. Inhibitory LSO neurons almost exclusively projected ipsilaterally making up a sizeable proportion (41%) of the transmitter type-labeled ipsilateral IC projection from LSO and exhibited a moderate low frequency bias (10% difference H-L). Two thirds of excitatory neurons projected contralaterally and had a slight high frequency bias (4%). One third of excitatory LSO neurons projected ipsilaterally to the IC and these cells were strongly biased toward the low frequency limb of the LSO (37%). This projection appears to be species specific in animals with good low frequency hearing suggesting that it may be a specialization for such ability.
Topics: Animals; Auditory Pathways; Brain Stem; Gerbillinae; Inferior Colliculi; Neurons; Superior Olivary Complex
PubMed: 34338321
DOI: 10.1002/cne.25226 -
Journal of Neurophysiology Sep 1998The precedence effect (PE) is experienced when two spatially separated sounds are presented with such a brief delay that only a single auditory image at or toward the...
The precedence effect (PE) is experienced when two spatially separated sounds are presented with such a brief delay that only a single auditory image at or toward the location of the leading source is perceived. The responses of neurons in the central nucleus of the inferior colliculus (ICC) of cats were studied using stimuli that are known to elicit the PE, focusing on the effects of changes in stimulus conditions that a listener might encounter in a natural situation. Experiments were conducted under both free-field (anechoic chamber) and dichotic (headphones) conditions. In free field, the PE was simulated by presenting two sounds from different loudspeakers with one sound delayed relative to the other. Either click or noise stimuli (2- to 10-ms duration) were used. Dichotically, the same conditions were simulated by presenting two click or noise pairs separated by an interstimulus delay (ISD) with interaural time differences (ITDs) imposed separately for each pair. At long ISDs, all neurons responded to both leading and lagging sources as if they were delivered alone. As the ISDs were shortened, the lagging response became suppressed. The ISD of half-maximal suppression varied considerably within the population of neurons studied, ranging from 2 to 100 ms, with means of 35 and 38 ms for free field and dichotic conditions, respectively. Several correlates of psychophysical findings were observed in ICC neurons: suppression was usually stronger with lower overall stimulus level and longer duration stimuli. Suppression also was compared along the azimuth and elevation in free field by placing the lagging source at (0 degree,0 degree), which is common to both axes, and the leading sources at locations along either plane that generated similar discharge rates. All neurons that showed suppression along the azimuth also did so in the elevation. In addition, there was a high correlation in the ISD of half-maximal suppression along the two planes (r = 0.87). These findings suggest that interaural difference cues, which are robust along the horizontal axis but minimal in the median plane, are not necessary for neural correlates of the PE to be manifested. Finally, single-neuron responses did not demonstrate a correlate of build-up of suppression, a phenomenon whereby echo suppression accumulates with ongoing stimulation. This finding adds credibility to theories about the PE that argue for a "higher order" component of the PE.
Topics: Animals; Auditory Perception; Auditory Threshold; Cats; Dichotic Listening Tests; Inferior Colliculi; Neurons, Afferent; Psychophysics; Reaction Time
PubMed: 9744939
DOI: 10.1152/jn.1998.80.3.1285 -
The European Journal of Neuroscience Jan 2017Extracting temporal periodicities and envelope shapes of sounds is important for listening within complex auditory scenes but declines behaviorally with age. Here, we...
Extracting temporal periodicities and envelope shapes of sounds is important for listening within complex auditory scenes but declines behaviorally with age. Here, we recorded local field potentials (LFPs) and spikes to investigate how ageing affects the neural representations of different modulation rates and envelope shapes in the inferior colliculus of rats. We specifically aimed to explore the input-output (LFP-spike) response transformations of inferior colliculus neurons. Our results show that envelope shapes up to 256-Hz modulation rates are represented in the neural synchronisation phase lags in younger and older animals. Critically, ageing was associated with (i) an enhanced gain in onset response magnitude from LFPs to spikes; (ii) an enhanced gain in neural synchronisation strength from LFPs to spikes for a low modulation rate (45 Hz); (iii) a decrease in LFP synchronisation strength for higher modulation rates (128 and 256 Hz) and (iv) changes in neural synchronisation strength to different envelope shapes. The current age-related changes are discussed in the context of an altered excitation-inhibition balance accompanying ageing.
Topics: Acoustic Stimulation; Action Potentials; Aging; Animals; Auditory Perception; Behavior, Animal; Inferior Colliculi; Neurons; Periodicity; Rats; Sound
PubMed: 27813207
DOI: 10.1111/ejn.13463 -
The Journal of Neuroscience : the... Jan 2010An important question in sensory neuroscience is what coding strategies and mechanisms are used by the brain to detect and discriminate among behaviorally relevant...
An important question in sensory neuroscience is what coding strategies and mechanisms are used by the brain to detect and discriminate among behaviorally relevant stimuli. There is evidence that sensory systems migrate from a distributed and redundant encoding strategy at the periphery to a more heterogeneous encoding in cortical structures. It has been hypothesized that heterogeneity is an efficient encoding strategy that minimizes the redundancy of the neural code and maximizes information throughput. Evidence of this mechanism has been documented in cortical structures. In this study, we examined whether heterogeneous encoding of complex sounds contributes to efficient encoding in the auditory midbrain by characterizing neural responses to behaviorally relevant vocalizations in the mouse inferior colliculus (IC). We independently manipulated the frequency, amplitude, duration, and harmonic structure of the vocalizations to create a suite of modified vocalizations. Based on measures of both spike rate and timing, we characterized the heterogeneity of neural responses to the natural vocalizations and their perturbed variants. Using information theoretic measures, we found that heterogeneous response properties of IC neurons contribute to efficient encoding of behaviorally relevant vocalizations.
Topics: Acoustic Stimulation; Action Potentials; Animals; Auditory Pathways; Auditory Perception; Brain Mapping; Female; Inferior Colliculi; Male; Mice; Mice, Inbred CBA; Models, Neurological; Neurons; Psychoacoustics; Spectrum Analysis; Statistics as Topic; Time Factors; Ultrasonics; Vocalization, Animal
PubMed: 20089889
DOI: 10.1523/JNEUROSCI.1964-09.2010 -
Neuron Mar 2012Both human speech and animal vocal signals contain frequency-modulated (FM) sounds. Although central auditory neurons that selectively respond to the direction of...
Both human speech and animal vocal signals contain frequency-modulated (FM) sounds. Although central auditory neurons that selectively respond to the direction of frequency modulation are known, the synaptic mechanisms underlying the generation of direction selectivity (DS) remain elusive. Here we show the emergence of DS neurons in the inferior colliculus by mapping the three major subcortical auditory nuclei. Cell-attached recordings reveal a highly reliable and precise firing of DS neurons to FM sweeps in a preferred direction. By using in vivo whole-cell current-clamp and voltage-clamp recordings, we found that the synaptic inputs to DS neurons are not direction selective, but temporally reversed excitatory and inhibitory synaptic inputs are evoked in response to opposing directions of FM sweeps. The construction of such temporal asymmetry, resulting DS, and its topography can be attributed to the spectral disparity of the excitatory and the inhibitory synaptic tonal receptive fields.
Topics: Action Potentials; Anesthetics, Local; Animals; Auditory Pathways; Biotin; Cesium; Cochlear Nucleus; Electric Stimulation; Female; Inferior Colliculi; Lidocaine; Patch-Clamp Techniques; Photic Stimulation; Potassium Channel Blockers; Rats; Rats, Sprague-Dawley; Sensory Receptor Cells; Sound Localization; Space Perception; Synaptic Transmission; Tetraethylammonium; Thalamus
PubMed: 22405210
DOI: 10.1016/j.neuron.2011.11.035 -
Respiratory Physiology & Neurobiology Jun 2016Threatening stimuli trigger rapid and coordinated behavioral responses supported by cardiorespiratory changes. The midbrain colliculi can generate coordinated orienting...
Threatening stimuli trigger rapid and coordinated behavioral responses supported by cardiorespiratory changes. The midbrain colliculi can generate coordinated orienting or defensive behavioral responses, and it has been proposed that collicular neurons also generate appropriate cardiovascular and respiratory responses to support such behaviors. We have shown previously that under conditions where collicular neurons are disinhibited, coordinated cardiovascular, somatomotor and respiratory responses can be evoked independently of the cortex by auditory, visual and somatosensory stimuli. Here we report that these natural stimuli effectively increase inspiratory time most likely though phase switching. As a result the pattern of phrenic and sympathetic coupling is an inspiratory-related sympathoexcitation. We propose that blockade of tonic GABAergic input in the midbrain colliculi permits alerting stimuli to drive command neurons that generate coordinated cardiovascular, respiratory and motor outputs. The outputs of these command neurons likely interact with the central respiratory pattern generator, however the precise output pathways mediating the coordinated autonomic and respiratory responses remain to be determined.
Topics: Animals; Autonomic Nervous System; Central Pattern Generators; Inferior Colliculi; Neurons; Respiration; Sensation; Superior Colliculi; gamma-Aminobutyric Acid
PubMed: 26563455
DOI: 10.1016/j.resp.2015.10.012 -
Journal of Neurophysiology Jul 2019Duration tuning in the mammalian inferior colliculus (IC) is created by the interaction of excitatory and inhibitory synaptic inputs. We used extracellular recordings...
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 (ISPL). We also measured rate-level functions of DTNs with single BD tones varied in SPL and modeled the excitatory half-maximum SPL (ESPL). There was a correlation between the ESPL and ISPL, 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. 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.
Topics: Animals; Auditory Threshold; Chiroptera; Evoked Potentials, Auditory; Excitatory Postsynaptic Potentials; Female; Inferior Colliculi; Inhibitory Postsynaptic Potentials; Male; Neurons; Reaction Time; Sound
PubMed: 31017836
DOI: 10.1152/jn.00653.2018 -
The Journal of Neuroscience : the... Jan 2014Duration-tuned neurons (DTNs) in the mammalian inferior colliculus (IC) arise from a combination of excitatory and inhibitory synaptic inputs. Previous research has...
Duration-tuned neurons (DTNs) in the mammalian inferior colliculus (IC) arise from a combination of excitatory and inhibitory synaptic inputs. Previous research has shown that the inhibition responsible for creating DTNs has a shorter latency than that of excitation and lasts longer than the stimulus duration. We used monotic and dichotic paired tone stimulation and recorded responses of DTNs from the IC of the bat to assess the relative contributions of each ear in forming duration-tuned circuits. The stimulus consisted of a short best duration (BD) excitatory tone and a longer duration nonexcitatory (NE) tone. In the monotic condition, when the BD and NE tones were presented to the contralateral ear and were sufficiently close in time, the NE tone always suppressed spikes evoked by the BD tone. In the dichotic condition, when the BD tone was presented to the contralateral ear and the NE tone to the ipsilateral ear, half of DTNs no longer showed spike suppression to the NE tone. Of those DTNs with suppression in both conditions, the latency of the inhibition was shorter and the duration of the inhibition was longer in the monotic condition. Therefore, in the monotic condition, DTNs received a contralaterally evoked inhibitory input that preceded the excitatory input to the same neuron. In the dichotic condition, DTNs received an ipsilaterally evoked inhibitory input that was weaker, longer in latency, and shorter in duration than the inputs from the contralateral ear. These findings indicate that the neural mechanisms that create DTNs in the IC are monaural.
Topics: Acoustic Stimulation; Animals; Auditory Perception; Chiroptera; Echolocation; Electrophysiology; Female; Inferior Colliculi; Male; Neurons
PubMed: 24403148
DOI: 10.1523/JNEUROSCI.3732-13.2014