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2. Glycinergic axonal inhibition subserves acute spatial sensitivity to sudden increases in sound intensity

Author

Tom P Franken, Brian J Bondy, David B Haimes, Joshua H Goldwyn, Nace L Golding, Philip H Smith, and Philip X Joris

Subjects
mongolian gerbil, temporal processing, sound localization, coincidence detection, glycine, axonal initial segment, Medicine, Science, Biology (General), QH301-705.5
Abstract

Locomotion generates adventitious sounds which enable detection and localization of predators and prey. Such sounds contain brisk changes or transients in amplitude. We investigated the hypothesis that ill-understood temporal specializations in binaural circuits subserve lateralization of such sound transients, based on different time of arrival at the ears (interaural time differences, ITDs). We find that Lateral Superior Olive (LSO) neurons show exquisite ITD-sensitivity, reflecting extreme precision and reliability of excitatory and inhibitory postsynaptic potentials, in contrast to Medial Superior Olive neurons, traditionally viewed as the ultimate ITD-detectors. In vivo, inhibition blocks LSO excitation over an extremely short window, which, in vitro, required synaptically evoked inhibition. Light and electron microscopy revealed inhibitory synapses on the axon initial segment as the structural basis of this observation. These results reveal a neural vetoing mechanism with extreme temporal and spatial precision and establish the LSO as the primary nucleus for binaural processing of sound transients.

Published
2021
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5. Physiological Diversity Influences Detection of Stimulus Envelope and Fine Structure in Neurons of the Medial Superior Olive

Author

Brian Bondy, David B. Haimes, and Nace L. Golding

Subjects
Sound localization, education.field_of_study, Topographic map (neuroanatomy), General Neuroscience, Sodium channel, Population, Stimulus (physiology), Biology, medicine.anatomical_structure, medicine, Neuron, Brainstem, education, Neuroscience, Research Articles, Envelope (waves)
Abstract

The neurons of the medial superior olive (MSO) of mammals extract azimuthal information from the delays between sounds reaching the two ears [interaural time differences (ITDs)]. Traditionally, all models of sound localization have assumed that MSO neurons represent a single population of cells with specialized and homogeneous intrinsic and synaptic properties that enable the detection of synaptic coincidence on a timescale of tens to hundreds of microseconds. Here, using patch-clamp recordings from large populations of anatomically labeled neurons in brainstem slices from male and female Mongolian gerbils (Meriones unguiculatus), we show that MSO neurons are far more physiologically diverse than previously appreciated, with properties that depend regionally on cell position along the topographic map of frequency. Despite exhibiting a similar morphology, neurons in the MSO exhibit subthreshold oscillations of differing magnitudes that drive action potentials at rates between 100 and 800 Hz. These oscillations are driven primarily by voltage-gated sodium channels and are distinct from resonant properties derived from other active membrane properties. We show that graded differences in these and other physiological properties across the MSO neuron population enable the MSO to duplex the encoding of ITD information in both fast, submillisecond time-varying signals as well as in slower envelopes. SIGNIFICANCE STATEMENT Neurons in the medial superior olive (MSO) encode sound localization cues by detecting microsecond differences in the arrival times of inputs from the left and right ears, and it has been assumed that this computation is made possible by highly stereotyped structural and physiological specializations. Here we report using a large (>400) sample size in which MSO neurons show a strikingly large continuum of functional properties despite exhibiting similar morphologies. We demonstrate that subthreshold oscillations mediated by voltage-gated Na(+) channels play a key role in conferring graded differences in firing properties. This functional diversity likely confers capabilities of processing both fast, submillisecond-scale synaptic activity (acoustic “fine structure”), and slow-rising envelope information that is found in amplitude-modulated sounds and speech patterns.

Published
2021

9. Glycinergic axonal inhibition subserves acute spatial sensitivity to sudden increases in sound intensity

Author

Brian Bondy, Nace L. Golding, David B. Haimes, Philip X. Joris, Philip H. Smith, Joshua H. Goldwyn, and Tom P. Franken

Subjects
Life Sciences & Biomedicine - Other Topics, Male, 0301 basic medicine, coincidence detection, mongolian gerbil, CONFIDENCE-INTERVALS, LATERAL SUPERIOR OLIVE, 0302 clinical medicine, Postsynaptic potential, axonal initial segment, Biology (General), NEURONS, Neurons, Physics, General Neuroscience, LOCALIZATION, sound localization, General Medicine, Excitatory postsynaptic potential, Medicine, Female, Life Sciences & Biomedicine, Research Article, Sound localization, QH301-705.5, MEDIAL NUCLEUS, Science, Olivary Nucleus, Inhibitory postsynaptic potential, General Biochemistry, Genetics and Molecular Biology, MECHANISMS, INITIAL SEGMENT, 03 medical and health sciences, Animals, DIFFERENCE SENSITIVITY, Biology, Science & Technology, INTERAURAL TIME DIFFERENCES, General Immunology and Microbiology, Excitatory Postsynaptic Potentials, temporal processing, Axon initial segment, Sound intensity, 030104 developmental biology, Inhibitory Postsynaptic Potentials, CELLS, Other, Gerbillinae, Neuroscience, Binaural recording, 030217 neurology & neurosurgery, glycine, Coincidence detection in neurobiology
Abstract

Locomotion generates adventitious sounds which enable detection and localization of predators and prey. Such sounds contain brisk changes or transients in amplitude. We investigated the hypothesis that ill-understood temporal specializations in binaural circuits subserve lateralization of such sound transients, based on different time of arrival at the ears (interaural time differences, ITDs). We find that Lateral Superior Olive (LSO) neurons show exquisite ITD-sensitivity, reflecting extreme precision and reliability of excitatory and inhibitory postsynaptic potentials, in contrast to Medial Superior Olive neurons, traditionally viewed as the ultimate ITD-detectors. In vivo, inhibition blocks LSO excitation over an extremely short window, which, in vitro, required synaptically evoked inhibition. Light and electron microscopy revealed inhibitory synapses on the axon initial segment as the structural basis of this observation. These results reveal a neural vetoing mechanism with extreme temporal and spatial precision and establish the LSO as the primary nucleus for binaural processing of sound transients. ispartof: ELIFE vol:10 ispartof: location:England status: published

Published
2021

10. De novo sequencing and initial annotation of the Mongolian gerbil (Meriones unguiculatus) genome

Author

Scott Monsma, Dan H. Sanes, Nace L. Golding, Edwin W. Rubel, Yuan Wang, and Diego A. R. Zorio

Subjects
Male, 0106 biological sciences, animal diseases, Gene prediction, Sequence assembly, Computational biology, Biology, Gerbil, 01 natural sciences, Genome, Article, 03 medical and health sciences, parasitic diseases, Genetics, Animals, Gene, 030304 developmental biology, Whole genome sequencing, 0303 health sciences, Base Sequence, Shotgun sequencing, Molecular Sequence Annotation, Sequence Analysis, DNA, nervous system, GenBank, sense organs, Gerbillinae, 010606 plant biology & botany
Abstract

The Mongolian gerbil ( Meriones unguiculatus ) is a member of the rodent family that displays several features not found in mice or rats, including sensory specializations and social patterns more similar to those in humans. These features have made gerbils a valuable animal for research studies of auditory and visual processing, brain development, learning and memory, and neurological disorders. Here, we report the whole gerbil annotated genome sequence, and identify important similarities and differences to the human and mouse genomes. We further analyze the chromosomal structure of eight genes with high relevance for controlling neural signaling and demonstrate a high degree of homology between these genes in mouse and gerbil. This homology increases the likelihood that individual genes can be rapidly identified in gerbil and used for genetic manipulations. The availability of the gerbil genome provides a foundation for advancing our knowledge towards understanding evolution, behavior and neural function in mammals. Accession number The Whole Genome Shotgun sequence data from this project has been deposited at DDBJ/ENA/GenBank under the accession NHTI00000000. The version described in this paper is version NHTI01000000. The fragment reads, and mate pair reads have been deposited in the Sequence Read Archive under BioSample accession SAMN06897401.

Published
2019

11. The relative contributions of MNTB and LNTB neurons to inhibition in the medial superior olive assessed through single and paired recordings

Author

Michael T Roberts, Stephanie C Seeman, and Nace L Golding

Subjects
Axons, Sound Localization, inhibition, timing, auditory brainstem, Neurosciences. Biological psychiatry. Neuropsychiatry, RC321-571
Abstract

The medial superior olive (MSO) senses microsecond differences in the coincidence of binaural signals, a critical cue for detecting sound location along the azimuth. An important component of this circuit is provided by inhibitory neurons of the medial and lateral nuclei of the trapezoid body (MNTB and LNTB, respectively). While MNTB neurons are fairly well described, little is known about the physiology of LNTB neurons. Using whole cell recordings from gerbil brainstem slices, we found that LNTB and MNTB neurons have similar membrane time constants and input resistances and fire brief action potentials, but only LNTB neurons fire repetitively in response to current steps. We observed that LNTB neurons receive graded excitatory and inhibitory synaptic inputs, with at least some of the latter arriving from other LNTB neurons. To address the relative timing of inhibition to the MSO from the LNTB vs. the MNTB, we examined inhibitory responses to auditory nerve stimulation using a slice preparation that retains the circuitry from the auditory nerve to the MSO intact. Despite the longer physical path length of excitatory inputs driving contralateral inhibition, inhibition from both pathways arrived with similar latency and jitter. An analysis of paired whole cell recordings between MSO and MNTB neurons revealed a short and reliable delay between the action potential peak in MNTB neurons and the onset of the resulting IPSP (0.55 ± 0.01 ms, n=4, mean ± SEM). Reconstructions of biocytin-labeled neurons showed that MNTB axons ranged from 580 to 858 µm in length (n=4). We conclude that while both LNTB and MNTB neurons provide similarly timed inhibition to MSO neurons, the reliability of inhibition from the LNTB at higher frequencies is more constrained relative to that from the MNTB due to differences in intrinsic properties, the strength of excitatory inputs, and the presence of feedforward inhibition.

Published
2014
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12. Excitatory cholecystokinin neurons of the midbrain integrate diverse temporal responses and drive auditory thalamic subdomains

Author

Preeti Mehta, Nace L. Golding, Boris V. Zemelman, Catherine J. Connelly, and Lauren J. Kreeger

Subjects
Inferior colliculus, Male, Auditory Pathways, Thalamus, Population, Optogenetics, Biology, Midbrain, inferior colliculus, Mesencephalon, medicine, Animals, medial geniculate, education, Neurons, education.field_of_study, Multidisciplinary, driver synapses, AAV, Biological Sciences, cholecystokinin, Electrophysiology, medicine.anatomical_structure, Receptive field, Evoked Potentials, Auditory, Female, Gerbillinae, Neuroscience, Nucleus
Abstract

Significance Our ability to identify sounds and understand communication signals depends upon our brains’ capacity to combine information about diverse sound features, including temporal patterns. The central nucleus of the inferior colliculus (ICC) performs an initial stage of this integration, but a circuit-based understanding of these processes has been hampered by difficulties in separating clearly defined functional cell types. Here we identify and characterize a major excitatory projection neuron of the ICC. These neurons show uniform intrinsic firing patterns and tuning to frequency, but strikingly diverse temporal responses to sound. Our results suggest that diversity in temporal coding is represented even within a single cell class and is likely primarily driven by differences in circuit connectivity., The central nucleus of the inferior colliculus (ICC) integrates information about different features of sound and then distributes this information to thalamocortical circuits. However, the lack of clear definitions of circuit elements in the ICC has limited our understanding of the nature of these circuit transformations. Here, we combine virus-based genetic access with electrophysiological and optogenetic approaches to identify a large family of excitatory, cholecystokinin-expressing thalamic projection neurons in the ICC of the Mongolian gerbil. We show that these neurons form a distinct cell type, displaying uniform morphology and intrinsic firing features, and provide powerful, spatially restricted excitation exclusively to the ventral auditory thalamus. In vivo, these neurons consistently exhibit V-shaped receptive field properties but strikingly diverse temporal responses to sound. Our results indicate that temporal response diversity is maintained within this population of otherwise uniform cells in the ICC and then relayed to cortex through spatially restricted thalamic subdomains.

Published
2021

17. Glycinergic axonal inhibition subserves acute spatial sensitivity to sudden increases in sound intensity

Author

Philip H. Smith, Philip X. Joris, Nace L. Golding, Brian Bondy, Tom P. Franken, and David B. Haimes

Subjects
Physics, media_common.quotation_subject, Inhibitory postsynaptic potential, Axon initial segment, Sound intensity, medicine.anatomical_structure, Postsynaptic potential, medicine, Excitatory postsynaptic potential, Contrast (vision), Nucleus, Neuroscience, Binaural recording, media_common
Abstract

Locomotion generates adventitious sounds which enable detection and localization of predators and prey. Such sounds contain brisk changes or transients in amplitude. We investigated the hypothesis that ill-understood temporal specializations in binaural circuits subserve lateralization of such sound transients, based on different time of arrival at the ears (interaural time differences, ITDs). We find that Lateral Superior Olive (LSO) neurons show exquisite ITD-sensitivity, reflecting extreme precision and reliability of excitatory and inhibitory postsynaptic potentials, in contrast to Medial Superior Olive neurons, traditionally viewed as the ultimate ITD-detectors. In vivo, inhibition blocks LSO excitation over an extremely short window, which, in vitro, required synaptically-evoked inhibition. Light and electron microscopy revealed inhibitory synapses on the axon initial segment as the structural basis of this observation. These results reveal a neural vetoing mechanism with extreme temporal and spatial precision and establish the LSO as the primary nucleus for binaural processing of sound transients.

Published
2020

22. Dendritic spikes as a mechanism for cooperative long-term potentiation

Author

Golding, Nace L., Staff, Nathan P., and Spruston, Nelson

Subjects
Environmental issues, Science and technology, Zoology and wildlife conservation
Abstract

Author(s): Nace L. Golding [1, 2]; Nathan P. Staff [2]; Nelson Spruston (corresponding author) Strengthening of synaptic connections following coincident pre- and postsynaptic activity was proposed by Hebb as a [...]

Published
2002
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26. SAT0459 EVALUATION OF THE PREVALENCE AND THE MANAGEMENT OF OSTEOPOROTIC FRACTURES IN PATIENTS HOSPITALIZED AT NANCY UNIVERSITY HOSPITAL (FRANCE) IN 2017.

Author

Baccichetti, A., primary, Nguyen-Thi, P. L., additional, Blum, A., additional, Mainard, D., additional, Sirveaux, F., additional, Nace, L., additional, Valance, A., additional, Civit, T., additional, Dautel, G., additional, Perret-Guillaume, C., additional, Guerci, B., additional, Tronel, H., additional, Chary Valckenaere, I., additional, and Loeuille, D., additional

Published
2020
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33. Shock III

Author

Siebenlist, D., Gattenlöhner, W., Lingnau, W., Hörmann, Ch, Putensen, Ch., Mutz, N., Jacquet, L., Jouret, J. C., Henin, P., Goenen, M., Tohmo, H., Karanko, M., Korpilahti, K., Scheinin, M., Viinamäki, O., Neuvonen, P., Sabatè, A., Sopena, R., Ramòn, R., Barcelò, E., Roqueta, C., Abad, A., Garcia, L., Garcia, X., Plaisance, P., Vicaut, E., Beloucif, S., Payen, D., Pasini, L., Ortalli, G., Sorbara, C., Lagonidis, D., Magder, S., Guardiola, J. J., Sarmiento, X., Alonso, S., Nigond J., Arich C., Bertinchant J. P., Bengler C., Stordeur J. M., Chandler, I. M., Stein, K. L., Gasior, T. A., Kormos, R. L., Pinsky, M. R., Fortuna, M., Horvat, M., Szabò, K., Burtin, P., Clavey, M., Mertès, P. M., Levy, B., Bischoff, N., Mathieu, P., Villemot, J. P., Haberer, J. P., El-Banayosy, A., Posival, H., Minami, K., Korner, M. M., Hartmann, D., Korfer, R., El-Banayosy, A., Kortke, H., Corbucci, G. G., Pohar, B., Osredkar, J., Kladnik, S., Bellinzona G., Noli S., Giordano A., Zlzzi S., Maestri M., Spada M., Raimondi M., Albertario F., Dionigi R. V., D’Orio, V., Martinez, C., Saad, G., Mendes, P., Marcelle, R., Staupach, K. H., Losser, M. R., Lenfant, F., Teisseire, B., Bollaert, P. E., Laterre, P. F., Audibert, G., Evenepoel, M., Lelarge, Ph., Larcan, A., Bauer, Ph., Nace, L., Laprevote-Heully, M. C., Larcan, A., Smithies, M. N., Yee, Tai Hwei, Jackson, L., Beale, R., Bihari, D. J., Alonso, C. Cisneros, Rodriguez, J. Gutierrez, Ramirez, F. SAnchez, Varela, J. Prados, Lòpez, P. Arribas, de la Gàndara, A. Martinez, Boiteau, R., Tenaillon, A., Lherm, T., Chamieh, F., Perrin-Gachadoat, D., Burdin, M., Masquelier, A. M., Capron, M. H., Dougnac, A., Andresen, M., Deckers, O., Evenepoel, H., Henin, D., Reynaert, M. S., Müller, C., Probst, S., Lischke, V., Nicovani, V., Hemàndez, G., Bavestrello, L., Castillo, L., Zhang, H., Sparen, H., Benlabed, M., Nuuyen, N., Vincent, J. L., Kunitz, O., Hillermann, T., Glöckner, P., Müller, F. G., and Kalff, G.

Published
1992
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36. In vivo coincidence detection in mammalian sound localization generates phase delays

Author

Tom P. Franken, Philip X. Joris, Nace L. Golding, Liting Wei, and Michael T. Roberts

Subjects
Sound localization, Male, Auditory Pathways, Patch-Clamp Techniques, Signal Detection, Psychological, Phase (waves), Biology, In Vitro Techniques, Gerbil, Coincidence, Article, Quinoxalines, medicine, otorhinolaryngologic diseases, Reaction Time, Auditory system, Animals, Detection theory, Psychoacoustics, Sound Localization, Neurons, Dose-Response Relationship, Drug, General Neuroscience, Brain, Excitatory Postsynaptic Potentials, Glycine Agents, Strychnine, medicine.anatomical_structure, Acoustic Stimulation, Female, Gerbillinae, Neuroscience, Excitatory Amino Acid Antagonists, Coincidence detection in neurobiology
Abstract

Sound localization critically depends on detection of differences in arrival time of sounds at the two ears (acoustic delay). The fundamental mechanisms are debated, but all proposals include a process of coincidence detection and a separate source of internal delay which offsets the acoustic delay and determines neural tuning. We obtained in vivo patch clamp recordings of binaural neurons in the Mongolian gerbil, combined with pharmacological manipulations, to directly compare neuronal input to output and to separate excitation from inhibition. The results cannot be accounted for by existing models and reveal that coincidence detection is not an instantaneous process but is shaped by the interaction of intrinsic conductances with preceding synaptic activity. This interaction generates an internal delay as an intrinsic part of the process of coincidence detection. The multiplication and time-shifting stages thought to extract synchronous activity in many brain areas can thus be combined in a single operation.

Published
2015

37. Amplitude Normalization of Dendritic EPSPs at the Soma of Binaural Coincidence Detector Neurons of the Medial Superior Olive

Author

Kenneth R. Ledford, Shan-Xue Jin, Nace L. Golding, and Bradley D. Winters

Subjects
0301 basic medicine, Sound localization, Male, Sensory Receptor Cells, Interaural time difference, Biology, Synapse, 03 medical and health sciences, 0302 clinical medicine, medicine, Animals, Sound Localization, Cells, Cultured, Research Articles, Dendritic spike, General Neuroscience, Excitatory Postsynaptic Potentials, Superior Olivary Complex, Dendrites, 030104 developmental biology, medicine.anatomical_structure, nervous system, Superior olivary complex, Synapses, Excitatory postsynaptic potential, Soma, Female, Gerbillinae, Neuroscience, 030217 neurology & neurosurgery, Coincidence detection in neurobiology
Abstract

The principal neurons of the medial superior olive (MSO) encode cues for horizontal sound localization through comparisons of the relative timing of EPSPs. To understand how the timing and amplitude of EPSPs are maintained during propagation in the dendrites, we made dendritic and somatic whole-cell recordings from MSO principal neurons in brain slices from Mongolian gerbils. In somatic recordings, EPSP amplitudes were largely uniform following minimal stimulation of excitatory synapses at visualized locations along the dendrites. Similar results were obtained when excitatory synaptic transmission was eliminated in a low calcium solution and then restored at specific dendritic sites by pairing input stimulation and focal application of a higher calcium solution. We performed dual dendritic and somatic whole-cell recordings to measure spontaneous EPSPs using a dual-channel template-matching algorithm to separate out those events initiated at or distal to the dendritic recording location. Local dendritic spontaneous EPSP amplitudes increased sharply in the dendrite with distance from the soma (length constant, 53.6 μm), but their attenuation during propagation resulted in a uniform amplitude of ∼0.2 mV at the soma. The amplitude gradient of dendritic EPSPs was also apparent in responses to injections of identical simulated excitatory synaptic currents in the dendrites. Compartmental models support the view that these results extensively reflect the influence of dendritic cable properties. With relatively few excitatory axons innervating MSO neurons, the normalization of dendritic EPSPs at the soma would increase the importance of input timing versus location during the processing of interaural time difference cuesin vivo.SIGNIFICANCE STATEMENTThe neurons of the medial superior olive analyze cues for sound localization by detecting the coincidence of binaural excitatory synaptic inputs distributed along the dendrites. Previous studies have shown that dendritic voltages undergo severe attenuation as they propagate to the soma, potentially reducing the influence of distal inputs. However, using dendritic and somatic patch recordings, we found that dendritic EPSP amplitude increased with distance from the soma, compensating for dendritic attenuation and normalizing EPSP amplitude at the soma. Much of this normalization reflected the influence of dendritic morphology. As different combinations of presynaptic axons may be active during consecutive cycles of sound stimuli, somatic EPSP normalization renders spike initiation more sensitive to synapse timing than dendritic location.

Published
2016

41. Synaptic integration in dendrites: exceptional need for speed

Author

Nace L. Golding and Donata Oertel

Subjects
Physiology, Synaptic integration, Posteroventral cochlear nucleus, Depolarization, Biology, medicine.anatomical_structure, nervous system, Coincident, medicine, Excitatory postsynaptic potential, Traveling wave, Auditory system, Medial superior olive, Neuroscience
Abstract

Some neurons in the mammalian auditory system are able to detect and report the coincident firing of inputs with remarkable temporal precision. A strong, low-voltage-activated potassium conductance (g(KL)) at the cell body and dendrites gives these neurons sensitivity to the rate of depolarization by EPSPs, allowing neurons to assess the coincidence of the rising slopes of unitary EPSPs. Two groups of neurons in the brain stem, octopus cells in the posteroventral cochlear nucleus and principal cells of the medial superior olive (MSO), extract acoustic information by assessing coincident firing of their inputs over a submillisecond timescale and convey that information at rates of up to 1000 spikes s(-1). Octopus cells detect the coincident activation of groups of auditory nerve fibres by broadband transient sounds, compensating for the travelling wave delay by dendritic filtering, while MSO neurons detect coincident activation of similarly tuned neurons from each of the two ears through separate dendritic tufts. Each makes use of filtering that is introduced by the spatial distribution of inputs on dendrites.

Published
2012

42. Serotonin modulates spike probability in the axon initial segment through HCN channels

Author

Kwang Woo Ko, Matthew N. Rasband, Nace L. Golding, Víctor M. Meseguer, and Richard H. Kramer

Subjects
0301 basic medicine, Serotonin, Patch-Clamp Techniques, Action Potentials, Cyclic Nucleotide-Gated Cation Channels, Sensory system, Serotonergic, Article, 03 medical and health sciences, 0302 clinical medicine, medicine, Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels, Animals, Channel blocker, Ion channel, Axon Initial Segment, Chemistry, General Neuroscience, Dendrites, Hyperpolarization (biology), Axon initial segment, Axons, 030104 developmental biology, medicine.anatomical_structure, nervous system, Soma, Neural coding, Gerbillinae, Neuroscience, 030217 neurology & neurosurgery
Abstract

The axon initial segment (AIS) serves as the site of action potential initiation in most neurons, but difficulties in isolating the effects of voltage-gated ion channels in the AIS from those of the soma and dendrites have hampered understanding how AIS properties influence neural coding. Here we have combined confocal microscopy, patch-clamp recordings and light-sensitive channel blockers ('photoswitches') in binaural auditory gerbil neurons to show that hyperpolarization and cyclic-nucleotide-gated (HCN) channels are expressed in the AIS and decrease spike probability, in a manner distinct from that of HCN channels in the soma and dendrites. Furthermore, the control of spike threshold by HCN channels in the AIS can be altered through serotonergic modulation of 5-hydroxytryptamine 1A (5-HT1A) receptors, which hyperpolarizes the activation range of HCN channels. As release of serotonin signals changes in motivation and attention states, axonal HCN channels provide a mechanism to translate these signals into changes in the threshold for sensory stimuli.

Published
2016

43. Glycinergic Inhibitory Plasticity in Binaural Neurons Is Cumulative and Gated by Developmental Changes in Action Potential Backpropagation

Author

Nace L. Golding and Bradley D. Winters

Subjects
Male, 0301 basic medicine, Sound localization, Action Potentials, Olivary Nucleus, Biology, Plasticity, Inhibitory postsynaptic potential, Article, 03 medical and health sciences, Receptors, Glycine, 0302 clinical medicine, Animals, Glycine receptor, Neurons, Neuronal Plasticity, General Neuroscience, Neural Inhibition, Long-term potentiation, Backpropagation, 030104 developmental biology, Inhibitory Postsynaptic Potentials, Female, Gerbillinae, Neuroscience, Binaural recording, 030217 neurology & neurosurgery, Coincidence detection in neurobiology
Abstract

Summary Utilization of timing-based sound localization cues by neurons in the medial superior olive (MSO) depends critically on glycinergic inhibitory inputs. After hearing onset, the strength and subcellular location of these inhibitory inputs are dramatically altered, but the cellular processes underlying this experience-dependent refinement are unknown. Here we reveal a form of inhibitory long-term potentiation (iLTP) in MSO neurons that is dependent on spiking and synaptic activation but is not affected by their fine-scale relative timing at higher frequencies prevalent in auditory circuits. We find that iLTP reinforces inhibitory inputs coactive with binaural excitation in a cumulative manner, likely well suited for networks featuring persistent high-frequency activity. We also show that a steep drop in action potential size and backpropagation limits induction of iLTP to the first 2 weeks of hearing. These intrinsic changes would deprive more distal inhibitory synapses of reinforcement, conceivably establishing the mature, soma-biased pattern of inhibition.

Published
2018

44. Control of submillisecond synaptic timing in binaural coincidence detectors by Kv1 channels

Author

Pablo E. Jercog, Nace L. Golding, John Rinzel, Paul J. Mathews, and Luisa L. Scott

Subjects
Patch-Clamp Techniques, Time Factors, Models, Neurological, Biophysics, Nonsynaptic plasticity, In Vitro Techniques, Biology, Article, Coincidence, Reaction Time, Animals, Patch clamp, Elapid Venoms, Neurons, General Neuroscience, Detector, Age Factors, Excitatory Postsynaptic Potentials, Dendrites, Electric Stimulation, Microsecond, Animals, Newborn, nervous system, Synapses, Shaker Superfamily of Potassium Channels, Excitatory postsynaptic potential, Gerbillinae, Neuroscience, Binaural recording, Brain Stem, Coding (social sciences)
Abstract

Neurons in the medial superior olive process sound-localization cues via binaural coincidence detection, in which excitatory synaptic inputs from each ear are segregated onto different branches of a bipolar dendritic structure and summed at the soma and axon with submillisecond time resolution. Although synaptic timing and dynamics critically shape this computation, synaptic interactions with intrinsic ion channels have received less attention. Using paired somatic and dendritic patch-clamp recordings in gerbil brainstem slices together with compartmental modeling, we found that activation of K(v)1 channels by dendritic excitatory postsynaptic potentials (EPSPs) accelerated membrane repolarization in a voltage-dependent manner and actively improved the time resolution of synaptic integration. We found that a somatically biased gradient of K(v)1 channels underlies the degree of compensation for passive cable filtering during propagation of EPSPs in dendrites. Thus, both the spatial distribution and properties of K(v)1 channels are important for preserving binaural synaptic timing.

Published
2010

46. Weak action potential backpropagation is associated with high-frequency axonal firing capability in principal neurons of the gerbil medial superior olive

Author

Travis A. Hage, Nace L. Golding, and Luisa L. Scott

Subjects
Physiology, Length constant, Neurotransmission, Biology, Neural backpropagation, Somatodendritic compartment, medicine.anatomical_structure, nervous system, medicine, Soma, Patch clamp, Axon, Neuroscience, Action potential initiation
Abstract

Principal neurons of the medial superior olive (MSO) convey azimuthal sound localization cues through modulation of their rate of action potential firing. Previous intracellular studies in vitro have shown that action potentials appear highly attenuated at the soma of MSO neurons, potentially reflecting specialized action potential initiation and/or a physically distant site of generation. To examine this more directly, we made dual patch-clamp recordings from MSO principal neurons in gerbil brainstem slices. Using somatic and dendritic whole-cell recordings, we show that graded action potentials at the soma are highly sensitive to the rate of rise of excitation and undergo strong attenuation in their backpropagation into the dendrites (length constant, 76 μm), particularly during strong dendritic excitation. Using paired somatic whole-cell and axonal loose-patch recordings, we show that action potentials recorded in the axon at distances > 25 μm are all-or-none, and uniform in amplitude even when action potentials appear graded at the soma. This proximal zone corresponded to the start of myelination in the axon, as assessed with immunocytochemical staining for myelin basic protein in single-labelled neurons. Finally, the axon was capable of sustaining remarkably high firing rates, with perfect entrainment occurring at frequencies of up to 1 kHz. Together, our findings show that action potential signalling in MSO principal neurons is highly secure, but shows a restricted invasion of the somatodendritic compartment of the cell. This restriction may be important for minimizing distortions in synaptic integration during the high frequencies of synaptic input encountered in the MSO.

Published
2007

47. Experimental shock

Author

Walmrath, D., Pilch, J., Grimminger, F., Seeger, W., Bollaert, P. E., Robin-Lherbier, B., Nace, L., Escanye, J. M., Mallie, J. P., Larcan, A., Haisjackl, M., Hasibeder, W., Sparr, H., Luz, G., Germann, R., Friesenecker, B., Schwarz, Ch., Tighe, D., Moss, R., Webb, A., Hayward, G., Al-Saady, N., Bennett, D., Nimmo, G. R., Cumming, A. D., Lamb, G., Hayward, G., and Wilson, A.

Published
1992
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48. Posthearing Developmental Refinement of Temporal Processing in Principal Neurons of the Medial Superior Olive

Author

Luisa L. Scott, Nace L. Golding, and Paul J. Mathews

Subjects
Sound localization, Dendrite, In Vitro Techniques, Olivary Nucleus, Biology, Hearing, medicine, Animals, Trapezoid body, Axon, Neurons, Membrane potential, General Neuroscience, Age Factors, Excitatory Postsynaptic Potentials, Electrophysiology, medicine.anatomical_structure, Animals, Newborn, nervous system, Time Perception, Auditory Perception, Excitatory postsynaptic potential, Soma, Gerbillinae, Neuroscience, Cellular/Molecular
Abstract

In mammals, principal neurons of the medial superior olive (MSO) exhibit biophysical specializations that enable them to detect sound localization cues with microsecond precision. In the present study, we used whole-cell patch recordings to examine the development of the intrinsic electrical properties of these neurons in brainstem slices from postnatal day 14 (P14) to P38 gerbils. In the week after hearing onset (P14–P21), we observed dramatic reductions in somatic EPSP duration, input resistance, and membrane time constant. Surprisingly, somatically recorded action potentials also dramatically declined in amplitude over a similar period (38 ± 3 to 17 ± 2 mV; τ = 5.2 d). Simultaneous somatic and dendritic patch recordings revealed that these action potentials were initiated in the axon, which primarily emerged from the soma. In older gerbils, the rapid speed of membrane voltage changes and the attenuation of action potential amplitudes were mediated extensively by low voltage-activated potassium channels containing the Kv1.1 subunit. In addition, whole-cell voltage-clamp recordings revealed that these potassium channels increase nearly fourfold from P14 to P23 and are thus a major component of developmental changes in excitability. Finally, the electrophysiological features of principal neurons of the medial nucleus of the trapezoid body did not change after P14, indicating that posthearing regulation of intrinsic membrane properties is not a general feature of all time-coding auditory neurons. We suggest that the striking electrical segregation of the axon from the soma and dendrites of MSO principal neurons minimizes spike-induced distortion of synaptic potentials and thus preserves the accuracy of binaural comparisons.

Published
2005

49. French Intensive Care Society, International congress - Réanimation 2016

Author

Jaillette, E, Girault, C, Brunin, G, Zerimech, F, Chiche, A, Broucqsault Dedrie, C, Fayolle, C, Minacori, F, Alves, I, Barrailler, S, Robriquet, L, Delaporte, E, Thellier, D, Delcourte, C, Duhamel, A, Nseir, S, Valette, X, Desmeulles, I, Savary, B, Masson, R, Seguin, A, Daubin, C, Sauneuf, B, Verrier, P, Pottier, V, Orabona, M, Samba, D, Viquesnel, G, Lermuzeaux, M, Hazera, P, Hanouz, J, Parienti, J, Du Cheyron, D, Demoule, A, Clavel, M, Rolland Debord, C, Perbet, S, Terzi, N, Kouatchet, A, Wallet, F, Roze, H, Vargas, F, Guérin, C, Dellamonica, J, Jaber, S, Similowski, T, Quenot, J, Binquet, C, Vinsonneau, C, Barbar, S, Vinault, S, Deckert, V, Lemaire, S, Hssain, A, Bruyère, R, Souweine, B, Lagrost, L, Adrie, C, Jung, B, Daurat, A, De Jong, A, Chanques, G, Mahul, M, Monnin, M, Molinari, N, Lheureux, O, Trepo, E, Hites, M, Cotton, F, Wolff, F, Surin, R, Créteur, J, Vincent, J, Gustot, T, Jacobs, F, Taccone, F, Neuville, M, Timsit, J, El Helali, N, Le Monnier, A, Magalhaes, E, Radjou, A, 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Elkhawand, C, Vermeesh, F, Vermeesh, F., and CITERIO, GIUSEPPE

Abstract

Determinants of outcome in critically ill patients with hematological malignancy and central neurological failure: data from the TRIAL OH study

Published
2016

50. Dendritic spikes as a mechanism for cooperative long-term potentiation

Author

Nathan P. Staff, Nace L. Golding, and Nelson Spruston

Subjects
Dendritic spike, Multidisciplinary, Post-tetanic potentiation, Pyramidal Cells, Long-Term Potentiation, Action Potentials, Excitatory Postsynaptic Potentials, Physiology, Nonsynaptic plasticity, Dendrites, Biology, Inhibitory postsynaptic potential, Neural backpropagation, Axons, Rats, Synaptic augmentation, Synapses, Synaptic plasticity, Biological neural network, Animals, Calcium, Calcium Signaling, Rats, Wistar, Theta Rhythm, Neuroscience
Abstract

Strengthening of synaptic connections following coincident pre- and postsynaptic activity was proposed by Hebb as a cellular mechanism for learning. Contemporary models assume that multiple synapses must act cooperatively to induce the postsynaptic activity required for hebbian synaptic plasticity. One mechanism for the implementation of this cooperation is action potential firing, which begins in the axon, but which can influence synaptic potentiation following active backpropagation into dendrites. Backpropagation is limited, however, and action potentials often fail to invade the most distal dendrites. Here we show that long-term potentiation of synapses on the distal dendrites of hippocampal CA1 pyramidal neurons does require cooperative synaptic inputs, but does not require axonal action potential firing and backpropagation. Rather, locally generated and spatially restricted regenerative potentials (dendritic spikes) contribute to the postsynaptic depolarization and calcium entry necessary to trigger potentiation of distal synapses. We find that this mechanism can also function at proximal synapses, suggesting that dendritic spikes participate generally in a form of synaptic potentiation that does not require postsynaptic action potential firing in the axon.

Published
2002

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