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Frontiers in Neural Circuits 2018Accurate perception of time-variant pitch is important for speech recognition, particularly for tonal languages with different lexical tones such as Mandarin, in which...
Accurate perception of time-variant pitch is important for speech recognition, particularly for tonal languages with different lexical tones such as Mandarin, in which different tones convey different semantic information. Previous studies reported that the auditory nerve and cochlear nucleus can encode different pitches through phase-locked neural activities. However, little is known about how the inferior colliculus (IC) encodes the time-variant periodicity pitch of natural speech. In this study, the Mandarin syllable /ba/ pronounced with four lexical tones (flat, rising, falling then rising and falling) were used as stimuli. Local field potentials (LFPs) and single neuron activity were simultaneously recorded from 90 sites within contralateral IC of six urethane-anesthetized and decerebrate guinea pigs in response to the four stimuli. Analysis of the temporal information of LFPs showed that 93% of the LFPs exhibited robust encoding of periodicity pitch. Pitch strength of LFPs derived from the autocorrelogram was significantly ( < 0.001) stronger for rising tones than flat and falling tones. Pitch strength are also significantly increased ( < 0.05) with the characteristic frequency (CF). On the other hand, only 47% (42 or 90) of single neuron activities were significantly synchronized to the fundamental frequency of the stimulus suggesting that the temporal spiking pattern of single IC neuron could encode the time variant periodicity pitch of speech robustly. The difference between the number of LFPs and single neurons that encode the time-variant F0 voice pitch supports the notion of a transition at the level of IC from direct temporal coding in the spike trains of individual neurons to other form of neural representation.
Topics: Acoustic Stimulation; Animals; China; Electroencephalography; Electrophysiological Phenomena; Female; Guinea Pigs; Inferior Colliculi; Male; Pitch Perception; Speech Perception
PubMed: 30087597
DOI: 10.3389/fncir.2018.00055 -
JASA Express Letters May 2024A long-standing quest in audition concerns understanding relations between behavioral measures and neural representations of changes in sound intensity. Here, we...
A long-standing quest in audition concerns understanding relations between behavioral measures and neural representations of changes in sound intensity. Here, we examined relations between aspects of intensity perception and central neural responses within the inferior colliculus of unanesthetized rabbits (by averaging the population's spike count/level functions). We found parallels between the population's neural output and: (1) how loudness grows with intensity; (2) how loudness grows with duration; (3) how discrimination of intensity improves with increasing sound level; (4) findings that intensity discrimination does not depend on duration; and (5) findings that duration discrimination is a constant fraction of base duration.
Topics: Animals; Rabbits; Loudness Perception; Inferior Colliculi; Acoustic Stimulation; Discrimination, Psychological; Auditory Perception; Neurons
PubMed: 38717467
DOI: 10.1121/10.0025874 -
Frontiers in Neural Circuits 2013Hierarchical processing of sensory information requires interaction at multiple levels along the peripheral to central pathway. Recent evidence suggests that interaction...
Hierarchical processing of sensory information requires interaction at multiple levels along the peripheral to central pathway. Recent evidence suggests that interaction between driving and modulating components can shape both top down and bottom up processing of sensory information. Here we show that a component inherited from extrinsic sources combines with local components to code sound intensity. By applying high concentrations of divalent cations to neurons in the nucleus of the inferior colliculus in the auditory midbrain, we show that as sound intensity increases, the source of synaptic efficacy changes from inherited inputs to local circuits. In neurons with a wide dynamic range response to intensity, inherited inputs increase firing rates at low sound intensities but saturate at mid-to-high intensities. Local circuits activate at high sound intensities and widen dynamic range by continuously increasing their output gain with intensity. Inherited inputs are necessary and sufficient to evoke tuned responses, however local circuits change peak output. Push-pull driving inhibition and excitation create net excitatory drive to intensity-variant neurons and tune neurons to intensity. Our results reveal that dynamic range and tuning re-emerge in the auditory midbrain through local circuits that are themselves variable or tuned.
Topics: Acoustic Stimulation; Animals; Auditory Pathways; Auditory Perception; Auditory Threshold; Inferior Colliculi; Mice; Neural Inhibition; Neurons
PubMed: 24198763
DOI: 10.3389/fncir.2013.00174 -
Neuroscience Oct 2016The central nucleus of the inferior colliculus (ICC) contains a laminar structure that functions as an organizing substrate of ascending inputs and local processing....
The central nucleus of the inferior colliculus (ICC) contains a laminar structure that functions as an organizing substrate of ascending inputs and local processing. While topographic distributions of ICC response parameters within and across laminae have been reported, the functional micro-organization of the ICC is less well understood. For pairs of neighboring ICC neurons, we examined the nature of functional connectivity and receptive field preferences to gain a better understanding of the structure and function of local circuits. By recording from pairs of adjacent neurons and presenting pure-tone and dynamic broad-band stimulation, we estimated functional connectivity and local differences in frequency response areas (FRAs), spectrotemporal receptive fields (STRFs), nonlinear input/output functions, and single-spike information. From the cross-covariance functions we identified putative unidirectional as well as bidirectional excitatory/inhibitory interactions. STRFs of neighboring neurons strongly conserve best frequency, and moderately agree in STRF similarity, bandwidth, temporal response type, best modulation frequency, nonlinearity structure, and degree of information processing. Excitatory connectivity was stronger and temporally more precise than for inhibitory connections. Neither connection strength nor degree of synchrony correlated with receptive field parameters. The functional similarity of local pairs of ICC neurons was substantially less than for local pairs in the granular layers of primary auditory cortex (AI). These results imply that while the ICC is an obligatory nexus of ascending information, local neurons are comparatively weakly connected and exhibit considerable receptive field variability, potentially reflecting the heterogeneity of converging inputs to ICC functional zones.
Topics: Acoustic Stimulation; Action Potentials; Animals; Auditory Cortex; Auditory Perception; Cats; Electrophysiology; Female; Inferior Colliculi; Models, Neurological; Nerve Net; Neurons; Time Factors
PubMed: 27544405
DOI: 10.1016/j.neuroscience.2016.08.024 -
The European Journal of Neuroscience Jan 2022How we distinguish multiple simultaneous stimuli is uncertain, particularly given that such stimuli sometimes recruit largely overlapping populations of neurons. One...
How we distinguish multiple simultaneous stimuli is uncertain, particularly given that such stimuli sometimes recruit largely overlapping populations of neurons. One commonly proposed hypothesis is that the sharpness of tuning curves might change to limit the number of stimuli driving any given neuron when multiple stimuli are present. To test this hypothesis, we recorded the activity of neurons in the inferior colliculus while monkeys made saccades to either one or two simultaneous sounds differing in frequency and spatial location. Although monkeys easily distinguished simultaneous sounds (~90% correct performance), the frequency selectivity of inferior colliculus neurons on dual-sound trials did not improve in any obvious way. Frequency selectivity was degraded on dual-sound trials compared to single-sound trials: neural response functions broadened and frequency accounted for less of the variance in firing rate. These changes in neural firing led a maximum-likelihood decoder to perform worse on dual-sound trials than on single-sound trials. These results fail to support the hypothesis that changes in frequency response functions serve to reduce the overlap in the representation of simultaneous sounds. Instead, these results suggest that alternative possibilities, such as recent evidence of alternations in firing rate between the rates corresponding to each of the two stimuli, offer a more promising approach.
Topics: Acoustic Stimulation; Animals; Inferior Colliculi; Macaca mulatta; Sound; Sound Localization
PubMed: 34844286
DOI: 10.1111/ejn.15545 -
The Journal of Comparative Neurology Jun 2017The inferior colliculus (IC) is the common target of separate pathways that transmit different types of auditory information. Beyond tonotopy, little is known about the...
The inferior colliculus (IC) is the common target of separate pathways that transmit different types of auditory information. Beyond tonotopy, little is known about the organization of response properties within the 3-dimensional layout of the auditory midbrain in most species. Through study of interaural time difference (ITD) processing, the functional properties of neurons can be readily characterized and related to specific pathways. To characterize the representation of ITDs relative to the frequency and hodological organization of the IC, the properties of neurons were recorded and the sites recovered histologically. Subdivisions of the IC were identified based on cytochrome oxidase (CO) histochemistry. The results were plotted within a framework formed by an MRI atlas of the gerbil brain. The central nucleus was composed of two parts, and lateral and dorsal cortical areas were identified. The lateral part of the central nucleus had the highest CO activity in the IC and a high proportion of neurons sensitive to ITDs. The medial portion had lower CO activity and fewer ITD-sensitive neurons. A common tonotopy with a dorsolateral to ventromedial gradient of low to high frequencies spanned the two regions. The distribution of physiological responses was in close agreement with known patterns of ascending inputs. An understanding of the 3-dimensional organization of the IC is needed to specify how the single tonotopic representation in the IC central nucleus leads to the multiple tonotopic representations in core areas of the auditory cortex.
Topics: Acoustic Stimulation; Action Potentials; Animals; Auditory Pathways; Brain Mapping; Cues; Electron Transport Complex IV; Female; Functional Laterality; Gerbillinae; Imaging, Three-Dimensional; Inferior Colliculi; Magnetic Resonance Imaging; Neurons; Psychoacoustics; Reaction Time; Time Factors
PubMed: 27997696
DOI: 10.1002/cne.24155 -
The Journal of Comparative Neurology Apr 2019The medial geniculate body (MG) receives a large input from the ipsilateral inferior colliculus (IC) and a smaller but substantial input from the contralateral IC. Both...
The medial geniculate body (MG) receives a large input from the ipsilateral inferior colliculus (IC) and a smaller but substantial input from the contralateral IC. Both crossed and uncrossed inputs comprise a large percentage of glutamatergic cells and a smaller percentage of GABAergic cells. We used double labeling with fluorescent retrograde tracers to identify individual IC cells that project bilaterally to the MGs in adult guinea pigs. We also used immunohistochemistry for glutamic acid decarboxylase to distinguish GABAergic from glutamatergic cells that project bilaterally to the MG. We found cells in the IC that contained both retrograde tracers, indicating that they project bilaterally. Across cases, the bilaterally projecting cells constituted up to 37% of the cells that project to the ipsilateral MG and up to 73% of the cells that project to the contralateral MG. GABAergic cells averaged 20% of the bilaterally-projecting population. We conclude that a population of IC cells sends branching axonal projections to innervate the MG bilaterally. Most of the neurons in this population are glutamatergic, with a minority that are GABAergic. A mixed projection, with glutamatergic cells outnumbering GABAergic cells, originates from each of the major IC subdivisions (central nucleus, dorsal cortex, and lateral cortex). The bilaterally projecting cells are likely to serve functions different from the larger unilateral projections, perhaps synchronizing activity on the two sides of the auditory brain.
Topics: Animals; Auditory Pathways; Female; Geniculate Bodies; Guinea Pigs; Inferior Colliculi; Male; Neurons
PubMed: 30536721
DOI: 10.1002/cne.24600 -
The Journal of Neuroscience : the... Apr 2022The dorsal cochlear nucleus (DCN) integrates auditory nerve input with nonauditory sensory signals and is proposed to function in sound source localization and...
The dorsal cochlear nucleus (DCN) integrates auditory nerve input with nonauditory sensory signals and is proposed to function in sound source localization and suppression of self-generated sounds. The DCN also integrates activity from descending auditory pathways, including a particularly large feedback projection from the inferior colliculus (IC), the main ascending target of the DCN. Understanding how these descending feedback signals are integrated into the DCN circuit and what role they play in hearing requires knowing the targeted DCN cell types and their postsynaptic responses. In order to explore these questions, neurons in the DCN that received descending synaptic input from the IC were labeled with a trans-synaptic viral approach in male and female mice, which allowed them to be targeted for whole-cell recording in acute brain slices. We tested their synaptic responses to optogenetic activation of the descending IC projection. Every cell type in the granule cell domain received monosynaptic, glutamatergic input from the IC, indicating that this region, considered an integrator of nonauditory sensory inputs, processes auditory input as well and may have complex and underappreciated roles in hearing. Additionally, we found that DCN cell types outside the granule cell regions also receive descending IC signals, including the principal projection neurons, as well as the neurons that inhibit them, leading to a circuit that may sharpen tuning through feedback excitation and lateral inhibition. Auditory processing starts in the cochlea and ascends through the dorsal cochlear nucleus (DCN) to the inferior colliculus (IC) and beyond. Here, we investigated the feedback projection from IC to DCN, whose synaptic targets and roles in auditory processing are unclear. We found that all cell types in the granule cell regions, which process multisensory feedback, also process this descending auditory feedback. Surprisingly, all except one cell type in the entire DCN receive IC input. The IC-DCN projection may therefore modulate the multisensory pathway as well as sharpen tuning and gate auditory signals that are sent to downstream areas. This excitatory feedback loop from DCN to IC and back to DCN could underlie hyperexcitability in DCN, widely considered an etiology of tinnitus.
Topics: Animals; Auditory Pathways; Axons; Cochlear Nucleus; Female; Inferior Colliculi; Male; Mice; Neurons
PubMed: 35273085
DOI: 10.1523/JNEUROSCI.1190-21.2022 -
American Journal of Physiology.... Sep 2012The superior and inferior colliculi are believed to generate immediate and highly coordinated defensive behavioral responses to threatening visual and auditory stimuli....
The superior and inferior colliculi are believed to generate immediate and highly coordinated defensive behavioral responses to threatening visual and auditory stimuli. Activation of neurons in the superior and inferior colliculi have been shown to evoke increases in cardiovascular and respiratory activity, which may be components of more generalized stereotyped behavioral responses. In this study, we examined the possibility that there are "command neurons" within the colliculi that can simultaneously drive sympathetic and respiratory outputs. In anesthetized rats, microinjections of bicuculline (a GABA(A) receptor antagonist) into sites within a circumscribed region in the deep layers of the superior colliculus and in the central and external nuclei of the inferior colliculus evoked a response characterized by intense and highly synchronized bursts of renal sympathetic nerve activity (RSNA) and phrenic nerve activity (PNA). Each burst of RSNA had a duration of ∼300-400 ms and occurred slightly later (peak to peak latency of 41 ± 8 ms) than the corresponding burst of PNA. The bursts of RSNA and PNA were also accompanied by transient increases in arterial pressure and, in most cases, heart rate. Synchronized bursts of RSNA and PNA were also evoked after neuromuscular blockade, artificial ventilation, and vagotomy and so were not dependent on afferent feedback from the lungs. We propose that the synchronized sympathetic-respiratory responses are driven by a common population of neurons, which may normally be activated by an acute threatening stimulus.
Topics: Animals; Bicuculline; Blood Pressure; GABA-A Receptor Antagonists; Heart; Heart Rate; Inferior Colliculi; Kidney; Male; Phrenic Nerve; Rats; Rats, Sprague-Dawley; Respiratory Physiological Phenomena; Superior Colliculi; Sympathetic Nervous System; Vasomotor System
PubMed: 22814668
DOI: 10.1152/ajpregu.00205.2012 -
ELife Oct 2019The 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...
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 two-photon Ca 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.
Topics: Acoustic Stimulation; Action Potentials; Animals; Auditory Pathways; Brain Mapping; Inferior Colliculi; Mice, Inbred C57BL; Neurons; Optical Imaging; Wakefulness
PubMed: 31612853
DOI: 10.7554/eLife.49091