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Auditory Brainstem Models: Adapting Cochlear Nuclei Improve Spatial Encoding by the Medial Superior Olive in Reverberation

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JARO-JOURNAL OF THE ASSOCIATION FOR RESEARCH IN OTOLARYNGOLOGY 2021年第3期22卷 289-318页

作者： Brughera, Andrew Mikiel-Hunter, Jason Dietz, Mathias McAlpine, David Macquarie Univ Dept Linguist Macquarie Pk NSW Australia Macquarie Univ Australian Hearing Hub Macquarie Pk NSW Australia Boston Univ Dept Biomed Engn Boston MA 02215 USA Carl von Ossietzky Univ Oldenburg Dept Med Phys & Akust Oldenburg Germany Carl von Ossietzky Univ Oldenburg Cluster Excellence Hearing4all Oldenburg Germany

Listeners typically perceive a sound as originating from the direction of its source, even as direct sound is followed milliseconds later by reflected sound from multiple different directions. Early-arriving sound is emphasised in the ascending auditory pathway, including the medial superior olive (MSO) where binaural neurons encode the interaural-time-difference (ITD) cue for spatial location. Perceptually, weighting of ITD conveyed during rising sound energy is stronger at 600 Hz than at 200 Hz, consistent with the minimum stimulus rate for binaural adaptation, and with the longer reverberation times at 600 Hz, compared with 200 Hz, in many natural outdoor environments. Here, we computationally explore the combined efficacy of adaptation prior to the binaural encoding of ITD cues, and excitatory binaural coincidence detection within MSO neurons, in emphasising ITDs conveyed in early-arriving sound. With excitatory inputs from adapting, nonlinear model spherical bushy cells (SBCs) of the bilateral cochlear nuclei, a nonlinear model MSO neuron with low-threshold potassium channels reproduces the rate-dependent emphasis of rising vs. peak sound energy in ITD encoding;adaptation is equally effective in the model MSO. Maintaining adaptation in model SBCs, and adjusting membrane speed in model MSO neurons, 'left' and 'right' populations of computationally efficient, linear model SBCs and MSO neurons reproduce this stronger weighting of ITD conveyed during rising sound energy at 600 Hz compared to 200 Hz. This hemispheric population model demonstrates a link between strong weighting of spatial information during rising sound energy, and correct unambiguous lateralisation of a speech source in reverberation.

关键词： adaptation cochlear nucleus MSO binaural sensory coding spatial hearing

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Echolocating bats rely on an innate speed-of-sound reference

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2021年第19期118卷 1页

作者： Amichai, Eran Yovel, Yossi Tel Aviv Univ Sch Zool IL-6997801 Tel Aviv Israel Dartmouth Coll Ecol Evolut Environm & Soc Grad Program Hanover NH 03766 USA Tel Aviv Univ Sagol Sch Neurosci IL-6997801 Tel Aviv Israel

Animals must encode fundamental physical relationships in their brains. A heron plunging its head underwater to skewer a fish must correct for light refraction, an archerfish shooting down an insect must "consider" gravity, and an echolocating bat that is attacking prey must account for the speed of sound in order to assess its distance. Do animals learn these relations or are they encoded innately and can they adjust them as adults are all open questions. We addressed this question by shifting the speed of sound and assessing the sensory behavior of a bat species that naturally experiences different speeds of sound. We found that both newborn pups and adults are unable to adjust to this shift, suggesting that the speed of sound is innately encoded in the bat brain. Moreover, our results suggest that bats encode the world in terms of time and do not translate time into distance. Our results shed light on the evolution of innate and flexible sensory perception.

关键词： sensory plasticity sensory coding sensory innateness echolocation target ranging

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Stimulus information guides the emergence of behavior-related signals in primary somatosensory cortex during learning

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CELL REPORTS 2024年第6期43卷 114244页

作者： Panniello, Mariangela Gillon, Colleen J. Maffulli, Roberto Celotto, Marco Richards, Blake A. Panzeri, Stefano Kohl, Michael M. Univ Oxford Dept Physiol Anat & Genet Oxford OX1 3PT England Univ Glasgow Sch Psychol & Neurosci Glasgow G12 8QQ Scotland Ist Italiano Tecnol Opt Approaches Brain Funct Lab I-16163 Genoa Italy Univ Toronto Scarborough Dept Biol Sci Toronto ON M1C 1A4 Canada Univ Toronto Dept Cell & Syst Biol Toronto ON M5S 3G5 Canada Mila Montreal PQ H2S 3H1 Canada Ist Italiano Tecnol Ctr Human Technol Neural Computat Lab I-16163 Genoa Italy Univ Med Ctr Hamburg Eppendorf UKE Inst Neural Informat Proc Ctr Mol Neurobiol ZMNH D-20251 Hamburg Germany Univ Bologna Dept Pharm & Biotechnol I-40126 Bologna Italy McGill Univ Sch Comp Sci Montreal PQ H3A 2A7 Canada McGill Univ Dept Neurol & Neurosurg Montreal PQ H3A 1A1 Canada Canadian Inst Adv Res Learning Machines & Brains Program Toronto ON M5G 1M1 Canada Montreal Neurol Inst Montreal PQ H3A 2B4 Canada

Neurons in the primary cortex carry sensory- and behavior -related information, but it remains an open question how this information emerges and intersects together during learning. Current evidence points to two possible learning -related changes: sensory information increases in the primary cortex or sensory information remains stable, but its readout efficiency in association cortices increases. We investigated this question by imaging neuronal activity in mouse primary somatosensory cortex before, during, and after learning of an object localization task. We quantified sensory- and behavior -related information and estimated how much sensory information was used to instruct perceptual choices as learning progressed. We find that sensory information increases from the start of training, while choice information is mostly present in the later stages of learning. Additionally, the readout of sensory information becomes more efficient with learning as early as in the primary sensory cortex. Together, our results highlight the importance of primary cortical neurons in perceptual learning.

关键词： mouse sensory coding decision-making two-photon imaging information theory

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Sensing fear: fast and precise threat evaluation in human sensory cortex

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TRENDS IN COGNITIVE SCIENCES 2023年第4期27卷 341-352页

作者： Li, Wen Keil, Andreas Florida State Univ Dept Psychol Tallahassee FL 32304 USA Univ Florida Dept Psychol Gainesville FL USA

Animal models of threat processing have evolved beyond the amygdala to incorpo-rate a distributed neural network. In human research, evidence has intensified in recent years to challenge the canonical threat circuitry centered on the amygdala, urging revision of threat conceptualization. A strong surge of research into threat processing in the sensory cortex in the past decade has generated particularly use-ful insights to inform the reconceptualization. Here, synthesizing findings from both animal and human research, we highlight sensitive, specific, and adaptable threat representations in the sensory cortex, arising from experience-based sculpting of sensory coding networks. We thus propose that the human sensory cortex can drive smart (fast and precise) threat evaluation, producing threat-imbued sensory afferents to elicit network-wide threat responses.

关键词： sensory coding threat representations threat conditioning associative plasticity long-term storage long-term memory

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Spike frequency adaptation facilitates the encoding of input gradient in insect olfactory projection neurons

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BIOSYSTEMS 2023年 223卷 104802页

作者： Lee, Hayeong Kostal, Lubomir Kanzaki, Ryohei Kobayashi, Ryota Univ Tokyo Sch Engn Tokyo 1138656 Japan Czech Acad Sci Inst Physiol Prague 14220 Czech Republic Univ Tokyo Res Ctr Adv Sci & Technol Tokyo 1538904 Japan Univ Tokyo Grad Sch Frontier Sci Kashiwa 2778561 Japan Univ Tokyo Math & Informat Ctr Tokyo 1138656 Japan JST PRESTO Saitama 3320012 Japan

The olfactory system in insects has evolved to process the dynamic changes in the concentration of food odors or sex pheromones to localize the nutrients or conspecific mating partners. Experimental studies have suggested that projection neurons (PNs) in insects encode not only the stimulus intensity but also its rate-of -change (input gradient). In this study, we aim to develop a simple computational model for a PN to understand the mechanism underlying the coding of the rate-of-change information. We show that the spike frequency adaptation is a potential key mechanism for reproducing the phasic response pattern of the PN in Drosophila. We also demonstrate that this adaptation mechanism enables the PN to encode the rate-of-change of the input firing rate. Finally, our model predicts that the PN exhibits the intensity-invariant response for the pulse and ramp odor stimulus. These results suggest that the developed model is useful for investigating the coding principle underlying olfactory information processing in insects.

关键词： Insect olfactory system Spike frequency adaptation Input rate-of-change sensory coding

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Co-transmitting interneurons in the mouse olfactory bulb regulate olfactory detection and discrimination

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CELL REPORTS 2023年第12期42卷 113471页

作者： Lyons-Warren, Ariel M. Tantry, Evelyne K. Moss, Elizabeth H. Kochukov, Mikhail Y. Belfort, Benjamin D. W. Ortiz-Guzman, Joshua Freyberg, Zachary Arenkiel, Benjamin R. Texas Childrens Hosp Jan & Dan Duncan Neurol Res Inst Baylor Coll Med Dept PediatSect Pediat Neurol & Dev Neurosci 1250 Moursund St Houston TX 77030 USA Texas Childrens Hosp Jan & Dan Duncan Neurol Res Inst Baylor Coll Med Dept Mol & Human Genet 1250 Moursund St Houston TX 77030 USA Baylor Coll Med Med Scientist Training Program 1 Baylor Plaza Houston TX 77030 USA Univ Pittsburgh Dept Psychiat Pittsburgh PA 15213 USA Univ Pittsburgh Dept Cell Biol Pittsburgh PA 15213 USA

Co-transmission of multiple neurotransmitters from a single neuron increases the complexity of signaling information within defined neuronal circuits. Superficial short-axon cells in the olfactory bulb release both dopamine and gamma-aminobutyric acid (GABA), yet the specific targets of these neurotransmitters and their respective roles in olfaction have remained unknown. Here, we implement intersectional genetics in mice to selectively block GABA or dopamine release from superficial short-axon cells to identify their distinct cellular targets, impact on circuit function, and behavioral contribution of each neurotransmitter toward olfactory behaviors. We provide functional and anatomical evidence for divergent superficial short-axon cell signaling onto downstream neurons to shape patterns of mitral cell firing that contribute to olfactory-related behaviors.

关键词： co-transmission olfaction sensory coding

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Sour taste: receptors, cells and circuits

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CURRENT OPINION IN PHYSIOLOGY 2021年 20卷 8-15页

作者： Liman, Emily R. Kinnamon, Sue C. Univ Southern Calif Dept Biol Sci Sect Neurobiol 3641 Watt Way Los Angeles CA 90089 USA Univ Colorado Dept Otolaryngol Anschutz Med Campus12700 E 19 Th Ave Aurora CO 80045 USA Univ Colorado Rocky Mt Taste & Smell Ctr Anschutz Med Campus12700 E 19 Th Ave Aurora CO 80045 USA

Sour taste, which is evoked by low pH, is one of the original four fundamental taste qualities, recognized as a distinct taste sensation for centuries, and universally aversive across diverse species. It is generally assumed to have evolved for detection of acids in unripe fruit and spoiled food. But despite decades of study, only recently have the receptor, the neurotransmitter, and the circuits for sour taste been identified. In this review, we describe studies leading up to the identification of the sour receptor as OTOP1, an ion channel that is selectively permeable to protons. We also describe advances in our understanding of how information is transmitted from the taste receptor cells to gustatory neurons, leading to behavioral aversion to acids.

关键词： OTOP1 Otopetrin PKD2L1 geniculate sensory coding serotonin sour taste trigeminal

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Amplitude modulation transfer functions reveal opposing populations within both the inferior colliculus and medial geniculate body

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JOURNAL OF NEUROPHYSIOLOGY 2020年第4期124卷 1198-1215页

作者： Kim, Duck O. Carney, Laurel Kuwada, Shigeyuki Univ Connecticut Ctr Hlth Dept Neurosci Farmington CT 06030 USA Univ Rochester Dept Biomed Engn Neurobiol & Anat Rochester NY USA

Based on single-unit recordings of modulation transfer functions (MTFs) in the inferior colliculus (IC) and the medial geniculate body (MGB) of the unanesthetized rabbit, we identified two opposing populations: band-enhanced (BE) and band-suppressed (BS) neurons. In response to amplitude-modulated (AM) sounds, firing rates of BE and BS neurons were enhanced and suppressed, respectively, relative to their responses to an unmodulated noise with a one-octave bandwidth. We also identified a third population, designated hybrid neurons, whose firing rates were enhanced by some modulation frequencies and sup- pressed by others. Our finding suggests that perception of AM may be based on the co-occurrence of enhancement and suppression of responses of the opposing populations of neurons. Because AM carries an important part of the content of speech, progress in understanding auditory processing of AM sounds should lead to progress in under- standing speech perception. Each of the BE, BS, and hybrid types of MTFs comprised approximately one-third of the total sample. Modulation envelopes having short duty cycles of 20-50% and raised- sine envelopes accentuated the degree of enhancement and suppression and sharpened tuning of the MTFs. With sinusoidal envelopes, peak modulation frequencies were centered around 32-64 Hz among IC BE neurons, whereas the MOB peak frequencies skewed toward lower frequencies, with a median of 16 Hz. We also tested an auditory-brain- stem model and found that a simple circuit containing fast excitatory synapses and slow inhibitory synapses was able to reproduce salient features of the BE- and BS-type MTFs of IC neurons. NEW & NOTEWORTHY Opposing populations of neurons have been identified in the mammalian auditory midbrain and thalamus. In response to amplitude-modulated sounds, responses of one population (band-enhanced) increased whereas responses of another (band-sup- pressed) decreased relative to their responses to an unmodulated sound. These o

关键词： auditory information processing sensory coding speech recognition temporal envelopes visual ON- and OFF-channels

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Theory of neuronal perturbome in cortical networks

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 2020年第43期117卷 26966-26976页

作者： Sadeh, Sadra Clopath, Claudia Imperial Coll London Bioengn Dept London SW7 2AZ England

To unravel the functional properties of the brain, we need to untangle how neurons interact with each other and coordinate in large-scale recurrent networks. One way to address this question is to measure the functional influence of individual neurons on each other by perturbing them in vivo. Application of such single-neuron perturbations in mouse visual cortex has recently revealed feature-specific suppression between excitatory neurons, despite the presence of highly specific excitatory connectivity, which was deemed to underlie feature-specific amplification. Here, we studied which connectivity profiles are consistent with these seemingly contradictory observations, by modeling the effect of single-neuron perturbations in large-scale neuronal networks. Our numerical simulations and mathematical analysis revealed that, contrary to the prima facie assumption, neither inhibition dominance nor broad inhibition alone were sufficient to explain the experimental findings;instead, strong and functionally specific excitatory-inhibitory connectivity was necessary, consistent with recent findings in the primary visual cortex of rodents. Such networks had a higher capacity to encode and decode natural images, and this was accompanied by the emergence of response gain nonlinearities at the population level. Our study provides a general computational framework to investigate how single-neuron perturbations are linked to cortical connectivity and sensory coding and paves the road to map the perturbome of neuronal networks in future studies.

关键词： neuronal perturbation cortical connectivity sensory coding visual cortex perturbome

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Decoding Cellular Mechanisms for Mechanosensory Discrimination

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NEURON 2021年第2期109卷 285-+页

作者： von Buchholtz, Lars J. Ghitani, Nima Lam, Ruby M. Licholai, Julia A. Chesler, Alexander T. Ryba, Nicholas J. P. Natl Inst Dent & Craniofacial Res NIH Bethesda MD 20892 USA Natl Ctr Complementary & Integrat Hlth Bethesda MD 20892 USA Brown Univ Brown Natl Inst Hlth Grad Partnerships Program Providence RI 02912 USA

Single-cell RNA-sequencing and in vivo functional imaging provide expansive but disconnected views of neuronal diversity. Here, we developed a strategy for linking these modes of classification to explore molecular and cellular mechanisms responsible for detecting and encoding touch. By broadly mapping function to neuronal class, we uncovered a clear transcriptomic logic responsible for the sensitivity and selectivity of mammalian mechanosensory neurons. Notably, cell types with divergent gene-expression profiles often shared very similar properties, but we also discovered transcriptomically related neurons with specialized and divergent functions. Applying our approach to knockout mice revealed that Piezo2 differentially tunes all types of mechanosensory neurons with marked cell-class dependence. Together, our data demonstrate how mechanical stimuli recruit characteristic ensembles of transcriptomically defined neurons, providing rules to help explain the discriminatory power of touch. We anticipate a similar approach could expose fundamental principles governing representation of information throughout the nervous system.

关键词： Touch sensory coding mechanosensation functional imaging spatial transcriptomics trigeminal system Piezo2 nociception somatosensation

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