Preferred Firing Phase Research Articles

Single-cell and ensemble activity of lumbar intermediate and ventral horn interneurons in the spinal air-stepping cat.

We explored the relationship between population interneuronal network activation and motor output in the adult, in vivo, air-stepping, spinal cat. By simultaneously measuring the activity of large numbers of spinal interneurons, we explored ensembles of coherently firing interneurons and their relation to motor output. In addition, the networks were analyzed in relation to their spatial distribution along the lumbar enlargement for evidence of localized groups driving particular phases of the locomotor step cycle. We simultaneously recorded hindlimb EMG activity during stepping and extracellular signals from 128 channels across two polytrodes inserted within lamina V-VII of two separate lumbar segments. Results indicated that spinal interneurons participate in one of two ensembles that are highly correlated with the flexor or the extensor muscle bursts during stepping. Interestingly, less than half of the isolated single units were significantly unimodally tuned during the step cycle whereas >97% of the single units of the ensembles were significantly correlated with muscle activity. These results show the importance of population scale analysis in neural studies of behavior as there is a much greater correlation between muscle activity and ensemble firing than between muscle activity and individual neurons. Finally, we show that there is no correlation between interneurons' rostrocaudal locations within the lumbar enlargement and their preferred phase of firing or ensemble participation. These findings indicate that spinal interneurons of lamina V-VII encoding for different phases of the locomotor cycle are spread throughout the lumbar enlargement in the adult spinal cord.NEW & NOTEWORTHY We report on the ensemble organization of interneuronal activity in the spinal cord during locomotor movements and show that lumbar intermediate zone interneurons organize in two groups related to the two major phases of walking: stance and swing. Ensemble organization is also shown to better correlate with muscular output than single-cell activity, although ensemble membership does not appear to be somatotopically organized within the spinal cord.

GABAergic Medial Septal Neurons with Low-Rhythmic Firing Innervating the Dentate Gyrus and Hippocampal Area CA3.

The medial septum implements cortical theta oscillations, a 5–12 Hz rhythm associated with locomotion and paradoxical sleep reflecting synchronization of neuronal assemblies such as place cell sequence coding. Highly rhythmic burst-firing parvalbumin-positive GABAergic medial septal neurons are strongly coupled to theta oscillations and target cortical GABAergic interneurons, contributing to coordination within one or several cortical regions. However, a large population of medial septal neurons of unidentified neurotransmitter phenotype and with unknown axonal target areas fire with a low degree of rhythmicity. We investigated whether low-rhythmic-firing neurons (LRNs) innervated similar or different cortical regions to high-rhythmic-firing neurons (HRNs) and assessed their temporal dynamics in awake male mice. The majority of LRNs were GABAergic and parvalbumin-immunonegative, some expressing calbindin; they innervated interneurons mostly in the dentate gyrus (DG) and CA3. Individual LRNs showed several distinct firing patterns during immobility and locomotion, forming a parallel inhibitory stream for the modulation of cortical interneurons. Despite their fluctuating firing rates, the preferred firing phase of LRNs during theta oscillations matched the highest firing probability phase of principal cells in the DG and CA3. In addition, as a population, LRNs were markedly suppressed during hippocampal sharp-wave ripples, had a low burst incidence, and several of them did not fire on all theta cycles. Therefore, CA3 receives GABAergic input from both HRNs and LRNs, but the DG receives mainly LRN input. We propose that distinct GABAergic LRNs contribute to changing the excitability of the DG and CA3 during memory discrimination via transient disinhibition of principal cells.SIGNIFICANCE STATEMENT For the encoding and recall of episodic memories, nerve cells in the cerebral cortex are activated in precisely timed sequences. Rhythmicity facilitates the coordination of neuronal activity and these rhythms are detected as oscillations of different frequencies such as 5–12 Hz theta oscillations. Degradation of these rhythms, such as through neurodegeneration, causes memory deficits. The medial septum, a part of the basal forebrain that innervates the hippocampal formation, contains high- and low-rhythmic-firing neurons (HRNs and LRNs, respectively), which may contribute differentially to cortical neuronal coordination. We discovered that GABAergic LRNs preferentially innervate the dentate gyrus and the CA3 area of the hippocampus, regions important for episodic memory. These neurons act in parallel with the HRNs mostly via transient inhibition of inhibitory neurons.

Ripple-related firing of identified deep CA1 pyramidal cells in chronic temporal lobe epilepsy in mice.

SummaryObjectiveTemporal lobe epilepsy (TLE) is often associated with memory deficits. Reactivation of memory traces in the hippocampus occurs during sharp‐wave ripples (SWRs; 140‐250 Hz). To better understand the mechanisms underlying high‐frequency oscillations and cognitive comorbidities in epilepsy, we evaluated how rigorously identified deep CA1 pyramidal cells (dPCs) discharge during SWRs in control and TLE mice.MethodsWe used the unilateral intraamygdala kainate model of TLE in video–electroencephalography (EEG) verified chronically epileptic adult mice. Local field potential and single‐cell recordings were performed using juxtacellular recordings from awake control and TLE mice resting on a spherical treadmill, followed by post hoc identification of the recorded cells.ResultsHippocampal SWRs in TLE mice occurred with increased intraripple frequency compared to control mice. The frequency of SWR events was decreased, whereas the overall frequency of SWRs, interictal epileptiform discharges, and high‐frequency ripples (250‐500 Hz) together was not altered. CA1 dPCs in TLE mice showed significantly increased firing during ripples as well as between the ripple events. The strength of ripple modulation of dPC discharges increased in TLE without alteration of the preferred phase of firing during the ripple waves.SignificanceThese juxtacellular electrophysiology data obtained from identified CA1 dPCs from chronically epileptic mice are in general agreement with recent findings indicating distortion of normal firing patterns during offline SWRs as a mechanism underlying deficits in memory consolidation in epilepsy. Because the primary seizure focus in our experiments was in the amygdala and we recorded from the CA1 region, these results are also in agreement with the presence of altered high‐frequency oscillations in areas of secondary seizure spread.

Single-unit Activity in the in vitro Entorhinal Cortex During Carbachol-induced Field Oscillations

The muscarinic receptor agonist carbachol (CCh) can induce activity in the theta range (4–15 Hz) in the entorhinal cortex (EC), but the underlying network mechanisms remain unclear. Here, we investigated the interplay between interneurons and principal cells in the EC during CCh-induced theta-like field oscillations in an in vitro brain slice preparation using tetrodes. Field oscillations at 10.1 Hz (IQR = 9.5–10.9 Hz) occurred during bath application of CCh (100 μM; n = 32 experiments) and were associated with single-unit (n = 189) firing. Interneuron activity increased before principal cell activity at the onset of the oscillations and both interneurons and principal cells fired at specific oscillation phases with interneurons preceding principal cells, suggesting that interneurons modulate principal cell activity during such oscillations. The regularity of occurrence of CCh-induced oscillations was abolished by applying the GABAA receptor antagonist picrotoxin (100 μM; n = 13). These effects were accompanied by changes in firing with principal cells discharging action potentials before interneurons, along with a loss of preferred firing phase for principal cells in relation to the oscillation peaks. Blocking ionotropic glutamatergic transmission abolished CCh-induced field oscillations (n = 6), suggesting that ionotropic glutamatergic receptor signaling is necessary for their generation. Our results show that neuronal network interactions leading to CCh-induced theta-like field oscillations rest on the close interplay between interneurons and principal cells and that interneurons modulate principal cell activity during such oscillatory activity. Moreover, they underscore the role of ionotropic glutamatergic transmission in this type of oscillations.

Task-Dependent Changes in Cross-Level Coupling between Single Neurons and Oscillatory Activity in Multiscale Networks

Understanding the principles governing the dynamic coordination of functional brain networks remains an important unmet goal within neuroscience. How do distributed ensembles of neurons transiently coordinate their activity across a variety of spatial and temporal scales? While a complete mechanistic account of this process remains elusive, evidence suggests that neuronal oscillations may play a key role in this process, with different rhythms influencing both local computation and long-range communication. To investigate this question, we recorded multiple single unit and local field potential (LFP) activity from microelectrode arrays implanted bilaterally in macaque motor areas. Monkeys performed a delayed center-out reach task either manually using their natural arm (Manual Control, MC) or under direct neural control through a brain-machine interface (Brain Control, BC). In accord with prior work, we found that the spiking activity of individual neurons is coupled to multiple aspects of the ongoing motor beta rhythm (10–45 Hz) during both MC and BC, with neurons exhibiting a diversity of coupling preferences. However, here we show that for identified single neurons, this beta-to-rate mapping can change in a reversible and task-dependent way. For example, as beta power increases, a given neuron may increase spiking during MC but decrease spiking during BC, or exhibit a reversible shift in the preferred phase of firing. The within-task stability of coupling, combined with the reversible cross-task changes in coupling, suggest that task-dependent changes in the beta-to-rate mapping play a role in the transient functional reorganization of neural ensembles. We characterize the range of task-dependent changes in the mapping from beta amplitude, phase, and inter-hemispheric phase differences to the spike rates of an ensemble of simultaneously-recorded neurons, and discuss the potential implications that dynamic remapping from oscillatory activity to spike rate and timing may hold for models of computation and communication in distributed functional brain networks.

Hippocampal CA1 pyramidal cells form functionally distinct sublayers

SummaryHippocampal CA1 pyramidal neurons have frequently been regarded as a homogeneous cell population in biophysical, pharmacological and modeling studies. Here we report robust differences between pyramidal neurons residing in the deep and superficial CA1 sublayers in the rat. Compared to their superficial peers, deep pyramidal cells fired at higher rates, burst more frequently, were more likely to have place fields and were more strongly modulated by slow oscillations of sleep. Both deep and superficial pyramidal cells fired preferentially at the trough of theta oscillations during maze exploration, yet during Rapid eye movement (REM) sleep, deep pyramidal cells shifted their preferred phase of firing to the peak of theta. Furthermore, whereas in waking, the majority of REM theta phase-shifting cells fired at the ascending phase of gamma oscillations, non-shifting cells preferred the trough. Thus, CA1 pyramidal cells in adjacent sublayers can address their targets jointly or differentially, depending on brain states.

Role of ICAN in rate, spike time, and theta phase coding by persistent spiking neurons of the medial entorhinal cortex

Persistent spiking neurons of the medial entorhinal cortex (mEC) exhibit bistability in that they are quiescent in the absence of synaptic or applied currents, but can be switched to a stable spiking state by a brief, strong depolarizing input. The spiking state is thought to be maintained by a positive feedback loop between a nonspecific calcium-sensitive cationic current (ICAN) carried by TRPC membrane channels and heightened intracellular calcium levels sustained during sufficiently fast spiking. Persistent spiking neurons in layer V of mEC are capable of sustaining a continuous range of stable spiking frequencies and can be switched to higher or lower frequencies by additional strong depolarizing or hyperpolarizing pulses, respectively1. This ability to generate graded persistent spiking has been hypothesized to underlie aspects of working memory, but it remains unclear if and to what extent persistent spiking is robust to the considerable fluctuating synaptic conductance that would be expected in vivo. Furthermore, the contribution of ICAN to the input-output processing of these neurons has not been evaluated. In this study we use a multi-compartmental GENESIS model of a layer V mEC neuron2 to investigate how ICAN might contribute to rate, spike time, and theta phase coding in these neurons. In the absence of synaptic inputs, we vary either an applied holding current or the magnitude of a 1 second current pulse delivered to the base model or to a version of the model from which ICAN has been removed. We then evaluate the spike frequency to applied current relationship at different time-points over the next 10 seconds. To explore the potential role of ICAN in spike time coding we deliver a 500 pA, 1 second current pulse during ongoing stochastic backgrounds composed of 1 nS AMPA and GABA synaptic events delivered to the soma. These backgrounds are intended to represent the in vivo high conductance state. We then evaluate the spike-triggered average (STA) of the CAN current before and after the pulse. We also derive the STAs of voltage (mean spike shape) and AMPA and GABA input conductances to evaluate how activation of ICAN might affect spike threshold and sensitivity to synaptic input fluctuations. Lastly, we delivered theta modulated synaptic input to the model and evaluate the preferred firing phase of the model for different levels of ICAN activation. We find that: 1) ICAN shapes the spike frequency to current relationship in a time-dependent manner; 2) The CAN current can support long-lasting elevated firing rates following strong excitation amidst ongoing stochastic synaptic activity; 3) Activation of the CAN current with a current pulse increases sensitivity to future synaptic input fluctuations; 4) Increased sensitivity is long-lasting and is greater for stronger pulses, allowing the CAN current to act as an intrinsic gain control mechanism.

Two distinct activity patterns of fast-spiking interneurons during neocortical UP states

During sleep, neocortical neuronal networks oscillate slowly (<1 Hz) between periods of activity (UP states) and silence (DOWN states). UP states favor the interaction between thalamic-generated spindles (7-14 Hz) and cortically generated gamma (30-80 Hz) waves. We studied how these three nested oscillations modulate fast-spiking interneuron (FSi) activity in vivo in VGAT-Venus transgenic rats. Our data describe a population of FSi that discharge "early" within UP states and another population that discharge "late." Early FSi tended to be silent during epochs of desynchronization, whereas late FSi were active. We hypothesize that late FSi may be responsible for generating the gamma oscillations associated with cognitive processing during wakefulness. Remarkably, FSi populations were differently modulated by spindle and gamma rhythms. Early FSi were robustly coupled to spindles and always discharged earlier than late FSi within spindle and gamma cycles. The preferred firing phase during spindle and gamma waves was strongly correlated in each cell, suggesting a cross-frequency coupling between oscillations. Our results suggest a precise spatiotemporal pattern of FSi activity during UP states, whereby information rapidly flows between early and late cells, initially promoted by spindles and efficiently extended by local gamma oscillations.

The Activity of Spinal Commissural Interneurons During Fictive Locomotion in the Lamprey

Commissural interneurons in the lamprey coordinate activity of the hemisegmental oscillators to ensure proper left-right alternation during swimming. The activity of interneuronal axons at the ventral commissure was studied together with potential target motoneurons during fictive locomotion in the isolated lamprey spinal cord. To estimate the unperturbed activity of the interneurons, axonal recordings were chosen because soma recordings inevitably will affect the level of membrane depolarization and thereby spike initiation. Of 227 commissural axons recorded during locomotor activity, 14 produced inhibitory and 3 produced excitatory postsynaptic potentials (PSPs) in target motoneurons. The axons typically fired multiple spikes per locomotor cycle, with approximately 10 Hz sustained frequency. The average shortest spike interval in a burst corresponded to an instantaneous frequency of approximately 50 Hz for both the excitatory and inhibitory axons. The maximum number of spikes per locomotor cycle was inversely related to the locomotor frequency, in accordance with previous observations in the spinal hemicord preparation. In axons that fired multiple spikes per cycle, the mean interspike intervals were in the range in which the amplitude of the slow afterhyperpolarization (sAHP) is large, providing further support for the role of the sAHP in spike timing. One hundred ninety-five axons (86%) fired rhythmically during fictive locomotion, with preferred phase of firing distributed over either the segmental locomotor burst phase (40% of axons) or the transitional phase (between bursts; 60%). Thus in lamprey commissural interneurons, we found a broad distribution of firing rates and phases during fictive locomotion.

Inhibitory synaptic plasticity regulates pyramidal neuron spiking in the rodent hippocampus

Spike-timing modifies the efficacy of both excitatory and inhibitory synapses onto CA1 pyramidal neurons in the rodent hippocampus. Repetitively spiking the presynaptic neuron before the postsynaptic neuron induces inhibitory synaptic plasticity, which results in a depolarization of the reversal potential for GABA (E GABA). Our goal was to determine how inhibitory synaptic plasticity regulates CA1 pyramidal neuron spiking in the rat hippocampus. We demonstrate electrophysiologically that depolarizing E GABA by 24.7 mV increased the spontaneous action potential firing frequency of cultured hippocampal neurons 254% from 0.12±0.07 Hz to 0.44±0.13 Hz ( n=11; P<0.05). Next we used a single compartment model of a CA1 pyramidal neuron to explore in detail how inhibitory synaptic plasticity of feedforward and feedback inhibition regulates the generation of action potentials, spike latency, and the minimum excitatory conductance required to generate an action potential; plasticity was modeled as a depolarization of E GABA, which effectively weakens inhibition. Depolarization of E GABA at feedforward and feedback inhibitory synapses decreased the latency to the 1st spike by 2.27 ms, which was greater that the sum of the decreases produced by depolarizing E GABA at feedforward (0.85 ms) or feedback inhibitory synapses (0.02 ms) alone. In response to a train of synaptic inputs, depolarizing E GABA decreased the inter-spike interval and increased the number of output spikes in a frequency dependent manner, improving the reliability of input–output transmission. Moreover, a depolarizing shift in E GABA at feedforward and feedback synapses triggered by spike trains recorded from CA1 pyramidal layer neurons during field theta from anesthetized rats, significantly increased spiking on the up- and down-strokes of the first half of the theta rhythm ( P<0.05), without changing the preferred phase of firing ( P=0.783). This study provides the first explanation of how depolarizing E GABA affects pyramidal cell output within the hippocampus.

Directionality of auditory nerve fiber responses to pure tone stimuli in the grassfrog, Rana temporaria . II. Spike timing

We studied the directionality of spike timing in the responses of single auditory nerve fibers of the grass frog, Rana temporaria, to tone burst stimulation. Both the latency of the first spike after stimulus onset and the preferred firing phase during the stimulus were studied. In addition, the directionality of the phase of eardrum vibrations was measured. The response latency showed systematic and statistically significant changes with sound direction at both low and high frequencies. The latency changes were correlated with response strength (spike rate) changes and were probably the result of directional changes in effective stimulus intensity. Systematic changes in the preferred firing phase were seen in all fibers that showed phaselocking (i.e., at frequencies below 500-700 Hz). The mean phase lead for stimulation from the contralateral side was approximately 140 degrees at 200 Hz and decreased to approximately 100 degrees at 700 Hz. These phaseshifts correspond to differences in spike timing of approximately 2 ms and 0.4 ms respectively. The phaseshifts were nearly independent of stimulus intensity. The phase directionality of eardrum vibrations was smaller than that of the nerve fibers. Hence, the strong directional phaseshifts shown by the nerve fibers probably reflect the directional characteristics of extratympanic pathways.

Directional masking of phase locking in the amphibian auditory nerve.

Directional masking in the amphibian auditory periphery was investigated by presenting frogs with a continuous tone from above and a continuous broadband noise from four different horizontal directions. This paradigm mimics the natural situation in which frogs are located in three-dimensional space and interference can and does arise from any direction. Intracellular recordings were made from single auditory-nerve fibers of the anesthetized adult leopard frogs using a dorsal approach. Vector strength (VS) and the mean preferred firing phase (MP) were measured for 94 low-frequency fibers. Thirty-six percent of the fibers demonstrated direction sensitivity of noise masking of VS. Most fibers exhibited a maximum decrease in VS at 90 degrees or 270 degrees noise incident angle and a minimum decrease in VS at 0 degrees or 180 degrees noise incident angle, suggesting higher noise susceptibility to the lateral fields than to the anterior or posterior field. Forty-nine percent of the fibers demonstrated direction sensitivity of noise masking of MP. Maximum shift in MP occurred most often at 90 degrees or 180 degrees noise incident angle, whereas minimum shift in MP occurred most frequently at 0 degrees or 270 degrees noise incident angle, suggesting higher noise susceptibility to the ipsilateral or posterior field than to the contralateral or anterior field. The difference in the directionality patterns of VS and MP suggests different mechanisms underlying noise masking of these two measures of phase locking in the amphibian auditory nerve.

Directionality of phase locking in auditory nerve fibers of the leopard frog Rana pipiens pipiens.

A dorsal approach to the eighth nerve and free-field stimulation were used to investigate the effect of sound direction and intensity on phase locking in auditory nerve fibers of the leopard frog Rana pipiens pipiens. Tuning curves of 75 auditory neurons were analyzed (Fig. 2). Amphibian papillar neurons, but not basilar papillar neurons, exhibit significant phase locking to short tone bursts at the characteristic frequency (CF), the degree of phase locking (vector strength) decreasing with the neuron's CF (Figs. 3, 4 and 10E). Vector strength increases with sound pressure level to saturate about 20 dB above threshold, while the preferred firing phase is only slightly affected (Figs. 5 and 6). In contrast, sound direction hardly affects vector strength (Figs. 7, 8, 9A and 10A and C), but has a strong influence on the preferred firing phase (Figs. 7, 8, 9B and C, 10B and D): With respect to anterior tone presentation there are phase lags for ipsilateral and phase leads for posterior and contralateral presentation. Phase differences between both ears show a sinusoidal or cardioid/ovoidal directional characteristic; maximum differences are found with antero-lateral tone presentation (Fig. 11). The directionality of phase locking decreases with the neuron's CF (Fig. 10F) and only slightly changes with sound pressure level (Fig. 12). Thus, phase locking of amphibian papilla neurons can potentially provide intensity-independent information for sound localization.

Firing relations of medial septal neurons to the hippocampal theta rhythm in urethane anesthetized rats.

On the basis of spontaneous firing patterns and relations to the hippocampal theta rhythm, three cell types were identified within the medial septal nucleus and vertical limb of the nucleus of the diagonal band of Broca (MSN-NDB). In addition to the well known rhythmically bursting cells that fired in bursts on each cycle of the hippocampal theta rhythm, two other cell types are distinguished. "Clock" cells fired at high rates with a very regular, periodic firing pattern that was unrelated to the theta rhythm. "Irregular" cells fired at much lower rates, especially during theta rhythm, and had a pseudo-random firing pattern. The firing of "irregular" cells was often significantly phase-locked to the hippocampal theta rhythm. Crude estimates of the relative proportions of these cell types suggest that the rhythmically bursting cells comprise about 75% of the cells of the MSN-NDB. These three cell types bear a remarkable resemblance, in firing patterns and relative proportions, to the three principal cell types of the medial septal nuclei described in the freely moving rat (Ranck 1976). Measurements of the preferred phases of firing of 128 rhythmically bursting septal neurons (including 22 atropine-resistant and 11 atropine-sensitive cells) indicate that there is no single preferred phase of firing for the population. Rather the distribution of phases over the theta cycle is statistically flat. Variations in recording locations cannot account for this distribution since large differences in preferred phase were found for pairs of cells at the same location. Similarly, plotting only the group of cells identified as projection cells by antidromic activation from the fimbria/fornix, failed to reveal a peak in the distribution. In contrast to the rhythmically bursting cells, the distribution of preferred firing phases for the "irregular" cells with a significant phase-locking to the theta rhythm did have a clear peak. The peak occurred near the dentate theta rhythm positivity, consistent with the hypothesis that they are driven by feedback from CA1 complex-spike cells.

Temporal response patterns of single auditory nerve fibers elicited by periodic electrical stimuli.

Single auditory nerve fibers exhibit firing synchronized to one or both phases of periodic AC stimulus currents. Responses to biphasic pulses depend on order and excitation sites of the two phases. Sine and triangle stimuli between 100 Hz and 500 Hz elicit similar response patterns. Responses to square waves are sometimes more synchronized and generally shifted in phase with respect to sine wave responses. Preferred firing phase(s): (1) are largely independent of stimulus intensity; (2) vary among fibers; (3) may shift continuously or discontinuously over several seconds before steady state is achieved. Responses to an unprocessed synthetic vowel stimulus were dominated by pitch period, first formant, and 'spurious' components.

Frequency and time domain comparison of low-frequency auditory fiber responses in two anuran amphibians

A comparative study of the phase-locked response of auditory nerve fibers was performed in two frog species, Eleutherodactylus coqui and Bombina orientalis. From the tuning characteristics and phase response of single auditory nerve fibers to low frequency tones (0.08–1.0 kHz) we attempt to deduce the mechanics of the auditory organ responsible for low-frequency hearing in the frog, the amphibian papilla (a.p.). The phase-locked responses of auditory nerve fibers in B. orientalis were essentially identical to those from cells with similar CFs in E. coqui, despite the presence of a conspicuous caudal extension of the a.p. in E. coqui (an apparently derived morphology), a feature completely absent in B. orientalis. The fine structure of the frequency-dependent phase behavior was examined in both species with a residual phase analysis. The most significant non-linear phase behavior was confined to neurons with CFs < 0.3 kHz. The intensity dependence of the phase response in E. coqui revealed that the preferred firing phase of an auditory nerve fiber depends upon the relation of test frequency (TF) and CF of the neuron examined. For TFs > CF there was a progressive phase lag as stimulus level was increased; the inverse was true for TFs < CF. Click latencies measured in E. coqui were inversely related to CF and were similar though systematically shorter than the response latencies estimated from the phase-frequency functions. The click response was similar to that documented in other species, showing a significant level dependence and the presence of multiple peaks, with the time between peaks related to the period of the neuron's CF. A ‘neurogram’ was compiled for a.p. fiber responses in both species in response to several pure tones. Based on the known tonotopy of the a.p. this measure reflects the phase response of the a.p. over the extent of its length. The population phase response in anurans is quite similar to that obtained from mammalian auditory nerve fibers for the same range of test frequencies (0.08–1.0 kHz). The similarity between the responses of auditory fibers in these two anuran species suggests the micromechanics of the a.p. rostral to the tectorial curtain is similar in both species and that it is the likely site for the origin of the CF-dependent time delays.

Frequency and intensity dependence of the preferred firing phase of starling cochlear ganglion cells

The preferred phase of firing of 28 cochlear ganglion cells in the anesthetized starling, was measured over a frequency range encompassing CF of typically 3 octaves and an intensity range of at least 30 dB. The phase versus frequency functions could be fit remarkably well by straight lines; the slopes of these functions represent the system delay between the stimulus onset and the occurrence of the spike at the recording electrode. After correction for acoustic and neural transmission, we find delays for tone stimuli of 90 dB SPL between 1.37 ms (for the highest-CF cells) and 2.40 ms (for the lowest CF cells). In addition, the slopes of the phase versus frequency functions, and hence the system delay, decrease with increasing stimulus intensity by 0.04 ms/dB. As in amphibians, reptiles, and mammals, the preferred phase of firing is nearly intensity-independent near CF, whereas increasing stimulus intensity above and below CF results in a progressive phase lead and lag, respectively. These results are discussed with respect to the underlying mechanisms of frequency analysis in the avian inner ear. [Work supported by the A.v. Humboldt Foundation, the SFB, and NIH.]