scholarly journals Contribution of action potentials to the extracellular field potential in the nucleus laminaris of barn owl

2018 ◽  
Vol 119 (4) ◽  
pp. 1422-1436 ◽  
Author(s):  
Paula T. Kuokkanen ◽  
Go Ashida ◽  
Anna Kraemer ◽  
Thomas McColgan ◽  
Kazuo Funabiki ◽  
...  

Extracellular field potentials (EFP) are widely used to evaluate in vivo neural activity, but identification of multiple sources and their relative contributions is often ambiguous, making the interpretation of the EFP difficult. We have therefore analyzed a model EFP from a simple brainstem circuit with separable pre- and postsynaptic components to determine whether we could isolate its sources. Our previous papers had shown that the barn owl neurophonic largely originates with spikes from input axons and synapses that terminate on the neurons in the nucleus laminaris (NL) (Kuokkanen PT, Wagner H, Ashida G, Carr CE, Kempter R. J Neurophysiol 104: 2274–2290, 2010; Kuokkanen PT, Ashida G, Carr CE, Wagner H, Kempter R. J Neurophysiol 110: 117–130, 2013; McColgan T, Liu J, Kuokkanen PT, Carr CE, Wagner H, Kempter R. eLife 6: e26106, 2017). To determine how much the postsynaptic NL neurons contributed to the neurophonic, we recorded EFP responses in NL in vivo. Power spectral analyses showed that a small spectral component of the evoked response, between 200 and 700 Hz, could be attributed to the NL neurons’ spikes, while nucleus magnocellularis (NM) spikes dominate the EFP at frequencies ≳1 kHz. Thus, spikes of NL neurons and NM axons contribute to the EFP in NL in distinct frequency bands. We conclude that if the spectral components of source types are different and if their activities can be selectively modulated, the identification of EFP sources is possible. NEW & NOTEWORTHY Extracellular field potentials (EFPs) generate clinically important signals, but their sources are incompletely understood. As a model, we have analyzed the auditory neurophonic in the barn owl’s nucleus laminaris. There the EFP originates predominantly from spiking in the afferent axons, with spectral power ≳1 kHz, while postsynaptic laminaris neurons contribute little. In conclusion, the identification of EFP sources is possible if they have different spectral components and if their activities can be modulated selectively.

1995 ◽  
Vol 268 (6) ◽  
pp. H2239-H2245 ◽  
Author(s):  
D. R. Grimm ◽  
R. E. DeMeersman ◽  
R. P. Garofano ◽  
A. M. Spungen ◽  
W. A. Bauman

This study investigated heart rate variability (HRV) in individuals with quadriplegia who have disruption of autonomic control of the heart. Seven male subjects with neurological complete quadriplegia and seven with incomplete quadriplegia were studied at rest and during provocation. HRV was measured by power spectral analysis using a fast Fourier transform. Two spectral components were generated: 1) the high-frequency (HF) peak, a reflection of parasympathetic activity, and 2) the low-frequency (LF) peak, primarily sympathetic activity with some parasympathetic input. Results of the provocative maneuvers were grouped into one composite variable. Significant differences in the LF spectral component were found between the groups with complete and incomplete lesions in the supine position and after provocation (LF supine: P = 0.01; LF provocation: P = 0.002). After provocation, significant differences were demonstrated in the HF spectral component between these groups (P = 0.005). In contrast to previous findings, a LF component in subjects with complete quadriplegia was observed; this LF component decreased after provocation, suggesting the parasympathetic component withdrew during stressful maneuvers. There also appeared to be general downregulation of parasympathetic activity to the heart in subjects with complete quadriplegia. The presence of an increased LF spectral component during provocation in those with incomplete lesions implies sympathetic stimulation of the heart and may be used as a marker of sympathetic activity in individuals with quadriplegia.


2015 ◽  
Vol 114 (3) ◽  
pp. 1862-1873 ◽  
Author(s):  
Catherine E. Carr ◽  
Sahil Shah ◽  
Thomas McColgan ◽  
Go Ashida ◽  
Paula T. Kuokkanen ◽  
...  

Axons from the nucleus magnocellularis form a presynaptic map of interaural time differences (ITDs) in the nucleus laminaris (NL). These inputs generate a field potential that varies systematically with recording position and can be used to measure the map of ITDs. In the barn owl, the representation of best ITD shifts with mediolateral position in NL, so as to form continuous, smoothly overlapping maps of ITD with iso-ITD contours that are not parallel to the NL border. Frontal space (0°) is, however, represented throughout and thus overrepresented with respect to the periphery. Measurements of presynaptic conduction delay, combined with a model of delay line conduction velocity, reveal that conduction delays can account for the mediolateral shifts in the map of ITD.


2015 ◽  
Vol 85 (4) ◽  
pp. 271-286 ◽  
Author(s):  
Nicolas Palanca-Castan ◽  
Christine Köppl

Localization of sound sources relies on 2 main binaural cues: interaural time differences (ITD) and interaural level differences. ITD computing is first carried out in tonotopically organized areas of the brainstem nucleus laminaris (NL) in birds and the medial superior olive (MSO) in mammals. The specific way in which ITD are derived was long assumed to conform to a delay line model in which arrays of systematically arranged cells create a representation of auditory space, with different cells responding maximally to specific ITD. This model conforms in many details to the particular case of the high-frequency regions (above 3 kHz) in the barn owl NL. However, data from recent studies in mammals are not consistent with a delay line model. A new model has been suggested in which neurons are not topographically arranged with respect to ITD and coding occurs through assessment of the overall response of 2 large neuron populations - 1 in each brainstem hemisphere. Currently available data comprise mainly low-frequency (<1,500 Hz) recordings in the case of mammals and higher-frequency recordings in the case of birds. This makes it impossible to distinguish between group-related adaptations and frequency-related adaptations. Here we report the first comprehensive data set from low-frequency NL in the barn owl and compare it to data from other avian and mammalian studies. Our data are consistent with a delay line model, so differences between ITD processing systems are more likely to have originated through divergent evolution of different vertebrate groups.


2018 ◽  
Vol 1 (4) ◽  
Author(s):  
Xiaoxin Wang ◽  
Ke Li ◽  
Lijuan Hou

Objective In this experiment, the Local field potential (LFPs) was observed in the substantia nigra compact and electrical activity change in corticostriatal pathway after D2DR intervention in exercise-induced fatigue rats. We analyzed the changes of DA neuron discharge and D2DR mediated corticostriatal pathway information transmission. To explore the mechanism of D2D2 mediated DA system in the information output of cortical M1 region. Methods Wistar rats were used to establish the model of exercise-induced fatigue. The rats were divided into control group (CG), 7 days fatigue group (7FG) and 24 hour recovery group (24RG). We used in vivo multichannel recording technology to record electrical activity in the M1, striatum and substantia nigra compact of rats and observed the electrophysiological changes after D2DR intervention. We also detected the expression of TH proteins in the dorsolateral striatum before and after exercise-induced fatigue by immunohistochemistry. Results 1) Compared with group CG, the expression of TH protein in the dorsolateral area of striatum was significantly decreased in group 7FG (P<0.05). 2) Compared with the CG group, the power spectral density of the θ, α and β band of the SNc was increased after seven days of exhaustion exercise(P < 0.05); After 24 hours of recovery, the PSD value decreased significantly compared with the 7FG group(P<0.05). 3)Compared with the CG group the power spectral density of alpha (7-13Hz) and beta (15-30Hz) bands in the M1 region and striatum was increased in 7FG after injection D2DR agonist(P < 0.05) . Conclusions After exercise-induced fatigue, the activity of substantia nigra was increased, and the activity of M1 and striatum was lower than that of the blank control group after the D2DR agonist  injection. As a key receptor for the DA signal system, D2DR regulates the electrical activity of the nigrostriatal DA pathway and affects the comprehensive information output of the cortex, which can be regarded as a target for exercise-induced fatigue (NSFC: 31401018,   SKXJX: 2014014, Corresponding [email protected]).


2010 ◽  
Vol 104 (4) ◽  
pp. 2274-2290 ◽  
Author(s):  
Paula T. Kuokkanen ◽  
Hermann Wagner ◽  
Go Ashida ◽  
Catherine E. Carr ◽  
Richard Kempter

The neurophonic is a sound-evoked, frequency-following potential that can be recorded extracellularly in nucleus laminaris of the barn owl. The origin of the neurophonic, and thus the mechanisms that give rise to its exceptional temporal precision, has not yet been identified. Putative generators of the neurophonic are the activity of afferent axons, synaptic activation of laminaris neurons, or action potentials in laminaris neurons. To identify the generators, we analyzed the neurophonic in the high-frequency (>2.5 kHz) region of nucleus laminaris in response to monaural pure-tone stimulation. The amplitude of the neurophonic is typically in the millivolt range. The signal-to-noise ratio reaches values beyond 30 dB. To assess which generators could give rise to these large, synchronous extracellular potentials, we developed a computational model. Spike trains were produced by an inhomogeneous Poisson process and convolved with a spike waveform. The model explained the dependence of the simulated neurophonic on parameters such as the mean rate, the vector strength of phase locking, the number of statistically independent sources, and why the signal-to-noise ratio is independent of the spike waveform and subsequent filtering of the signal. We found that several hundred sources are needed to reach the observed signal-to-noise ratio. The summed coherent signal from the densely packed afferent axons and activation of their synapses on laminaris neurons are alone sufficient to explain the measured properties of the neurophonic.


2007 ◽  
Vol 98 (3) ◽  
pp. 1697-1705 ◽  
Author(s):  
Fredrik Bengtsson ◽  
Henrik Jörntell

The last few years have seen an increase in the variety of in vivo experiments used for studying cerebellar physiological mechanisms. A combination of ketamine and xylazine has become a particularly popular form of anesthesia. However, because nonanesthetized control conditions are lacking in these experiments, so far there has been no evaluation of the effects of these drugs on the physiological activity in the cerebellar neuronal network. In the present study, we used the mossy fiber, parallel fiber, and climbing fiber field potentials evoked in the nonanesthetized, decerebrated rat to serve as a control condition against which the effects of intravenous drug injections could be compared. All anesthetics were applied at doses required for normal maintenance of anesthesia. We found that ketamine substantially depressed the evoked N3 field potential, which is an indicator of the activity in the parallel fiber synapses (−40%), and nearly completely abolished evoked climbing fiber field potentials (−90%). Xylazine severely depressed the N3 field (−75%) and completely abolished the climbing fiber field (−100%). In a combination commonly used for general anesthesia (20:1), ketamine–xylazine injections also severely depressed the N3 field (−75%) and nearly completely abolished the climbing fiber field (−90%). We also observed that lowered body and surface temperatures (<34°C) resulted in a substantial depression of the N3 field (−50%). These results urge for some caution in the interpretations of studies on cerebellar network physiology performed in animals anesthetized with these drugs.


2019 ◽  
Vol 121 (3) ◽  
pp. 1034-1047
Author(s):  
Thomas McColgan ◽  
Paula T. Kuokkanen ◽  
Catherine E. Carr ◽  
Richard Kempter

Synaptic currents are frequently assumed to make a major contribution to the extracellular field potential (EFP). However, in any neuronal population, the explicit separation of synaptic sources from other contributions such as postsynaptic spikes remains a challenge. Here we take advantage of the simple organization of the barn owl nucleus laminaris (NL) in the auditory brain stem to isolate synaptic currents through the iontophoretic application of the α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-receptor antagonist 1,2,3,4-tetrahydro-6-nitro-2,3-dioxo-benzo[ f]quinoxaline-7-sulfonamide (NBQX). Responses to auditory stimulation show that the temporal dynamics of the evoked synaptic contributions to the EFP are consistent with synaptic short-term depression (STD). The estimated time constants of an STD model fitted to the data are similar to the fast time constants reported from in vitro experiments in the chick. Overall, the putative synaptic EFPs in the barn owl NL are significant but small (<1% change of the variance by NBQX). This result supports the hypothesis that the EFP in NL is generated mainly by axonal spikes, in contrast to most other neuronal systems. NEW & NOTEWORTHY Synaptic currents are assumed to make a major contribution to the extracellular field potential in the brain, but it is hard to directly isolate these synaptic components. Here we take advantage of the simple organization of the barn owl nucleus laminaris in the auditory brain stem to isolate synaptic currents through the iontophoretic application of a synaptic blocker. We show that the responses are consistent with a simple model of short-term synaptic depression.


1993 ◽  
Vol 69 (4) ◽  
pp. 1276-1291 ◽  
Author(s):  
D. A. Prince ◽  
G. F. Tseng

1. Field potentials and intracellular activities were examined in neocortical slices obtained through areas of chronic cortical injury produced by cortical undercutting and transcortical lesions made in vivo 7-122 days before the terminal in vitro slice experiment. 2. Abnormal field potentials characterized by long- and variable-latency multiphasic events could be evoked by layer VI-white matter or subpial stimulation in 9 of 15 animals that had adequate partial cortical isolations. These "epileptiform" field potentials were recorded in layers II-V and propagated across the cortex. They appeared at threshold in an all-or-none fashion and, in most slices, could be blocked by increasing stimulus intensity. In one slice, spontaneous epileptiform events occurred that were similar to those evoked by extracellular stimulation. 3. Intracellular activities during the epileptiform field potentials consisted of polyphasic synaptic events that were predominantly depolarizing and that could last < or = 400-500 ms, synchronous with the field potential activities. A variety of observations suggested that the neuronal activities underlying epileptiform field potentials were relatively asynchronous and much less intense than those previously found in chemically induced epileptogenesis within the neocortex. 4. Inhibitory postsynaptic potentials (IPSPs) were not prominent in neurons when threshold stimuli evoked epileptiform events; however, suprathreshold stimuli could elicit biphasic IPSPs and block the long-latency polysynaptic activity and abnormal field potential in most slices. Depolarizing components of the polysynaptic activity had the appearance of excitatory postsynaptic potentials in terms of their responses to alterations in membrane potential. 5. Comparison of spike parameters in layer V neurons of epileptogenic slices with those in control layer V neurons showed no significant differences in spike height, threshold, duration, or rise time. Resting membrane potentials were also not significantly different. 6. There was a highly significant difference in input resistance (RN) between layer V neurons in control and injured slices; the mean value for neurons in lesioned cortex was 68.1 M omega, whereas that in control cells was 30.5 M omega. There was also a significant prolongation of the slow membrane time constant in neurons of injured cortex (19.4 ms) as opposed to that in control cells (12.2 ms), suggesting that a change in specific resistivity or capacitance contributed to the higher RNS. 7. The relationship between adapted spike frequency and applied current (f-I slope) was steeper in layer V neurons from injured cortical slices (44.3 Hz/nA) than in normal layer V cells (28.2 Hz/nA).(ABSTRACT TRUNCATED AT 400 WORDS)


2013 ◽  
Vol 33 (12) ◽  
pp. 1937-1943 ◽  
Author(s):  
Luka R Srejic ◽  
William D Hutchison ◽  
Michelle M Aarts

Since the most significant ischemic sequelae occur within hours of stroke, it is necessary to understand how neuronal function changes during this time. While histologic and behavioral models show the extent of stroke-related damage, only in vivo recordings can illustrate changes in brain activity during stroke and validate effectiveness of neuroprotective compounds. Spontaneous and evoked field potentials (fEPs) were recorded in the deep layers of the cortex with a linear microelectrode array for 3 hours after focal stroke in anesthetized rats. Tat-NR2B9c peptide, which confers neuroprotection by uncoupling the PSD-95 protein from N-methyl-D-aspartate receptor (NMDAR), was administered 5 minutes before ischemia. Evoked field potentials were completely suppressed within 3 minutes of infarct in all ischemic groups. Evoked field potential recovery after stroke in rats treated with Tat-NR2B9c (83% of baseline) was greater compared with stroke-only (61% of baseline) or control peptide (Tat-NR2B-AA; 67% of baseline) groups ( P<0.001). Electroencephalography (EEG) power was higher in Tat-NR2B9c-treated animals at both 20 minutes and 1 hour (50% and 73% of baseline, respectively) compared with stroke-only and Tat-NR2B-AA-treated rats ( P<0.05). Tat-NR2B9c significantly reduces stroke-related cortical dysfunction as evidenced by greater recovery of fEPs and EEG power; illustrating the immediate effects of the compound on poststroke brain function.


2018 ◽  
Author(s):  
Alexandra P. Chatzikalymniou ◽  
Frances K. Skinner

AbstractOscillations in local field potentials (LFPs) commonly occur and analyses of them fuel brain function hypotheses. An understanding of the cellular correlates and pathways affecting LFPs is needed but many overlapping pathways in vivo makes this difficult to achieve. A prevalent LFP rhythm in the hippocampus is ‘theta’ (3-12 Hz). Theta rhythms emerge intrinsically in an in vitro whole hippocampus preparation and thus can be produced by local interactions between interneurons and pyramidal (PYR) cells. Overlapping pathways are much reduced in this preparation making it possible to decipher the contribution of different cell types to LFP generation. We focus on oriens-lacunosum/moleculare (OLM) cells as a major class of interneurons in the hippocampus. They can influence PYR cells through two distinct pathways, (i) by direct inhibition of PYR cell distal dendrites, and (ii) by indirect disinhibition of PYR cell proximal dendrites by inhibiting bistratified cells (BiCs) that target them. We use previous inhibitory network models and build biophysical LFP models using volume conductor theory. We assess the effect of OLM cells to ongoing intrinsic LFP theta rhythms by directly comparing our model LFP features with experiment. We find that robust LFP theta responses adhering to reproducible experimental criteria occur only for particular connectivities between OLM cells and BiCs. Decomposition of the LFP reveals that OLM cell inputs onto the PYR cell regulate robustness of LFP responses without affecting average power and that the robust response depends on co-activation of distal inhibition and basal excitation. We use our models to estimate the spatial extent of the region generating LFP theta rhythms, leading us to predict that about 22,000 PYR cells participate in generating the LFP theta rhythm. Besides allowing us to understand OLM cells’ contributions to intrinsic theta rhythms, our work can drive hypothesis developments of cellular contributions in vivo.Author SummaryOscillatory local field potentials (LFPs) are extracellularly recorded potentials that are widely used to interpret information processing in the brain. For example, theta LFP rhythms (3-12 Hz) are correlated with memory processing and it is known that particular inhibitory cell types control their existence. As such, it is critical for us to appreciate how various cell types contribute to the characteristics of LFP rhythms. A precise biophysical modeling scheme linking activity at the cellular level and the recorded signal has been established. However, it is difficult to assess cellular contributions in vivo because of many spatiotemporally overlapping pathways that prevent the unambiguous separation of signals. Using an in vitro preparation that exhibits intrinsic theta (3-12 Hz) rhythms and where there is much less overlap, we build biophysical LFP models to explore cell contributions to ongoing intrinsic theta rhythms. We uncover distinct contributions from different cell types and show that robust theta rhythms depend specifically on one of the cell types. We are able to determine this because our LFP models have direct links with experiment and we are able to perform thousands of simulations.


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