scholarly journals Enhancement of phase-locking in rodents. I. An axonal recording study in gerbil

2017 ◽  
Vol 118 (4) ◽  
pp. 2009-2023 ◽  
Author(s):  
Liting Wei ◽  
Shotaro Karino ◽  
Eric Verschooten ◽  
Philip X. Joris

The trapezoid body (TB) contains axons of neurons in the anteroventral cochlear nucleus projecting to monaural and binaural nuclei in the superior olivary complex (SOC). Characterization of these monaural inputs is important for the interpretation of response properties of SOC neurons. In particular, understanding of the sensitivity to interaural time differences (ITDs) in neurons of the medial and lateral superior olive requires knowledge of the temporal firing properties of the monaural excitatory and inhibitory inputs to these neurons. In recent years, studies of ITD sensitivity of SOC neurons have made increasing use of small animal models with good low-frequency hearing, particularly the gerbil. We presented stimuli as used in binaural studies to monaural neurons in the TB and studied their temporal coding. We found that general trends as have been described in the cat are present in gerbil, but with some important differences. Phase-locking to pure tones tends to be higher in TB axons and in neurons of the medial nucleus of the TB (MNTB) than in the auditory nerve for neurons with characteristic frequencies (CFs) below 1 kHz, but this enhancement is quantitatively more modest than in cat. Stronger enhancement is common when TB neurons are stimulated at low frequencies below CF. It is rare for TB neurons in gerbil to entrain to low-frequency stimuli, i.e., to discharge a well-timed spike on every stimulus cycle. Also, complex phase-locking behavior, with multiple modes of increased firing probability per stimulus cycle, is common in response to low frequencies below CF. NEW & NOTEWORTHY Phase-locking is an important property of neurons in the early auditory pathway: it is critical for the sensitivity to time differences between the two ears enabling spatial hearing. Studies in cat have shown an improvement in phase-locking from the peripheral to the central auditory nervous system. We recorded from axons in an output tract of the cochlear nucleus and show that a similar but more limited form of temporal enhancement is present in gerbil.

1989 ◽  
Vol 61 (2) ◽  
pp. 257-268 ◽  
Author(s):  
R. Batra ◽  
S. Kuwada ◽  
T. R. Stanford

1. The difference in the time of arrival of a sound at the two ears can be used to locate its source along the azimuth. Traditionally, it has been thought that only the on-going interaural temporal disparities (ITDs) produced by sounds of lower frequency (approximately less than 2 kHz) could be used for this purpose. However, ongoing ITDs of low frequency are also produced by envelopes of amplitude-modulated (AM) tones. These ITDs can be detected and used to lateralize complex high-frequency sounds (1, 8, 12, 15, 22, 24, 26). Auditory neurons synchronize to the modulation envelope, but do so at progressively lower modulation frequencies at higher levels of the auditory pathway. Some neurons of the cochlear nucleus synchronize best to frequencies as high as 700 Hz, but those of the inferior colliculus (IC) exhibit their best synchrony below 200 Hz. Even though synchrony to higher modulation frequencies is reduced at higher levels of the auditory pathway, is information about ITDs retained? 2. We answered this question by extracellularly recording the responses of neurons in the IC of the unanesthetized rabbit. We used an unanesthetized preparation because anesthesia alters the responses of neurons in the IC to both monaurally presented tones and ITDs. The unanesthetized rabbit is ideal for auditory research. Recordings can be maintained for long periods, and the acoustic stimulus to each ear can be independently controlled. 3. We studied the responses of 89 units to sinusoidally AM tones presented to the contralateral ear. For each unit, we recorded the response at several modulation frequencies. The degree of phase locking to the envelope at each frequency was measured using the synchronization coefficient. Two measures were used to assess the range of modulation frequencies over which phase locking occurred. The "best AM frequency" was the frequency at which we observed the greatest phase locking. The "highest AM frequency" was the highest frequency at which significant phase locking (0.001 level) was observed. We could not assess synchrony to ipsilateral AM tones directly, because most units did not respond to ipsilateral stimulation. 4. We studied the sensitivity of 63 units to ITDs produced by the envelopes of AM tones. Sensitivity to ITDs was tested by presenting AM tones to the two ears that had the same carrier frequency, but modulation frequencies that differed by 1 Hz. Units that were sensitive to ITDs responded to this stimulus by varying their response rate cyclically at the difference frequency, i.e., 1 Hz.(ABSTRACT TRUNCATED AT 400 WORDS)


2022 ◽  
Author(s):  
Saman Abbaspoor ◽  
Ahmed Hussin ◽  
Kari L Hoffman

Nested hippocampal oscillations in the rodent gives rise to temporal coding that may underlie learning, memory, and decision making. Theta/gamma coupling in rodent CA1 occurs during exploration and sharp-wave ripples during quiescence. Whether these oscillatory regimes extend to primates is less clear. We therefore sought to identify correspondences in frequency bands, nesting, and behavioral coupling taken from macaque hippocampus. We found that, in contrast to the rodent, theta and gamma frequency bands in macaque CA1 were segregated by behavioral states. Beta/gamma (15-70Hz) had greater power during visual search while theta (7-10 Hz) dominated during quiescence. Moreover, delta/theta (3-8 Hz) amplitude was strongest when beta2/slow gamma (20-35 Hz) amplitude was weakest, though the low frequencies coupled with higher, ripple frequencies (60-150 Hz). The distribution of spike-field coherence revealed three peaks matching the 3-10 Hz, 20-30 Hz and 60-150 Hz bands; however, the low frequency effects were primarily due to sharp-wave ripples. Accordingly, no intrinsic theta spiking rhythmicity was apparent. These results support a role for beta2/slow gamma modulation in CA1 during active exploration in the primate that is decoupled from theta oscillations. These findings diverge from the rodent oscillatory canon and call for a shift in focus and frequency when considering the primate hippocampus.


1978 ◽  
Vol 41 (6) ◽  
pp. 1557-1559 ◽  
Author(s):  
J. F. Brugge ◽  
E. Javel ◽  
L. M. Kitzes

1. Responses to pure tones were recorded from single neurons in the anteroventral cochlear nucleus (AVCN) in kittens ranging in age from 4 to 45 days. Different response properties mature at different times after birth. 2. The shapes of response areas of AVCN neurons after the 1st postnatal week resemble those recorded in the AVCN and auditory nerve of the adult. During the 1st wk after birth the high-frequency portion of the response area is extended. Phase-locked responses to stimulus frequencies below about 600 Hz occur at this time. Phase vs. frequency measurements and shapes of response areas indicate that by the end of the 1st postnatal week the cochlear partition may be capable of supporting a traveling wave along most of its length. 3. Functional development proceeds through a second phase which lasts until the end of the 2nd or the beginning of the 3rd wk of life. During that time threshold, maximal discharge rate, and average first-spike latency achieve adult values. 4. Phase-locking to low-frequency tones, to the extent displayed by phase-sensitive neurons in the adult AVCN or auditory nerve, is achieved last, after the 3rd or 4th wk postpartum.


2002 ◽  
Vol 87 (6) ◽  
pp. 2915-2928 ◽  
Author(s):  
Oliver Behrend ◽  
Antje Brand ◽  
Christoph Kapfer ◽  
Benedikt Grothe

The ascending auditory pathway is characterized by parallel processing. At the brain stem level, several structures are involved that are known to serve different well-defined functions. However, the function of one prominent brain stem nucleus, the rodent superior paraolivary nucleus (SPN) and its putative homologue in other mammals, the dorsomedial periolivary nucleus, is unknown. Based on extracellular recordings from anesthetized gerbils, we tested the role of the SPN in sound localization and temporal processing. First, the existence of binaural inputs indicates that the SPN might be involved in sound localization. Although almost half of the neurons exhibited binaural interactions (most of them excited from both sides), effects of interaural time and intensity differences (ITD; IID) were weak and ambiguous. Thus a straightforward function of SPN in sound localization appears to be implausible. Second, inputs from octopus and multipolar/stellate cells of the cochlear nucleus and from principal cells of the medial nucleus of the trapezoid body could relate to precise temporal processing in the SPN. Based on discharge types, two subpopulations of SPN cells were observed: about 60% of the neurons responded to pure tones with sustained discharges, with irregular spike patterns and no phase-locking. Only four neurons showed a regular spike pattern (“chopping”). About 40% of the neurons responded with phasic on or off discharges. Average first spike latency observed in neurons with sustained discharges was significantly shorter than that of on responders, but had a considerably higher trial-to-trial variation (“jitter”). A subpopulation of on responders showed a jitter of less than ±0.1 ms. Most neurons (66%) responded to sinusoidally amplitude-modulated sounds (SAM) with an ongoing response, phase-locked to the stimulus envelope. Again, on responders showed a significantly higher temporal precision in the phase-locked discharge compared with the sustained responders. High variability was observed among spike-rate-based modulation transfer functions. Histologically, a massive concentration of cytochemical markers for glycinergic input to SPN cells was demonstrated. Application of glycine or its blockade revealed profound effects of glycinergic inhibition on the auditory responses of SPN neurons. The existence of at least two subpopulations of neurons is in line with different subsets of SPN cells that can be distinguished morphologically. One temporally less precise population might modulate the processing of its target structures by providing a rather diffuse inhibition. In contrast, precise onresponders might provide a short, initial inhibitory pulse to its targets.


1994 ◽  
Vol 71 (3) ◽  
pp. 1037-1051 ◽  
Author(s):  
P. X. Joris ◽  
P. H. Smith ◽  
T. C. Yin

1. Discharges of neurons in the peripheral auditory system contain information about the temporal features of acoustic stimuli. Phase-locking of neurons in the anteroventral cochlear nucleus (AVCN) is usually reported to be less robust than in auditory nerve (AN) fibers, which provide their major input. In a companion paper we reported that some cells in AVCN of the cat show enhanced phase-locking compared with the AN when stimulated at the frequency to which they are most sensitive [characteristic frequency (CF)]. We called neurons "high-sync" when they showed vector strengths (R, a measure of phase-locking) > or = 0.9. Here we report phase-locking properties to stimuli at frequencies below CF. 2. Horseradish peroxidase-filled glass micropipettes or metal microelectrodes were inserted into the trapezoid body (TB), which is the large output tract of the AVCN. Acoustically driven fibers were classified on the basis of the shape of the poststimulus time (PST) histograms to short tone bursts at CF. We then presented low-frequency tones of increasing SPL and determined the maximum R value at 500 Hz (R500) for each fiber. Using the same experimental protocol we studied phase-locking in the ANs of two animals because maximal R values at the tuning curve tail have not been reported for AN fibers. 3. Although phase-locking in AN fibers is usually assumed to be independent of CF, we found that fibers with CF > 2 kHz tended to have higher R500 values than fibers with CF < or = 2 kHz. Moreover, R500 was > or = 0.9 in 20% (42 of 196) of the fibers studied and could be as high as 0.95. This population of fibers was defined as having "high-sync tails" and consisted almost entirely of fibers with low or medium spontaneous rate. 4. High-CF TB fibers stimulated at 500 Hz showed very high phase-locking. High-sync tails (R500 > or = 0.9) were found in 41 of 70 TB fibers. For a subset of these fibers (1/3 in total: 23 of 70) phase-locking was higher than is ever observed in the AN (R500 > or = 0.95); these fibers were defined as showing synchronization "enhancement." Virtually all fibers showing synchronization enhancement had primary-like-with-notch (PLN) PST histograms. Chopper and primary-like fibers showed high-sync tails for CFs > 3 kHz. 5. Synchronization filter functions were obtained for high-CF AN fibers by determining maximum synchronization for a range of stimuli below CF.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 72 (5) ◽  
pp. 2209-2221 ◽  
Author(s):  
A. S. Feng ◽  
W. Y. Lin

1. We made extracellular recordings from 164 single neurons in the frog dorsal medullary nucleus (DMN), a homologue of the cochlear nucleus. Phase-locked responses to tones at the unit's characteristic frequency (CF) and to off-CF tones were evaluated. We also stimulated units with tones at CF that were amplitude modulated sinusoidally between 5 and 1,000 Hz and examined responses to these stimuli. 2. Results showed that single neurons in the frog DMN displayed phase-locked discharges to tones at frequencies < or = 800 Hz. Phase-locking was robust at low frequencies (< 400 Hz) and became poorer at higher frequencies; the variation of the synchronization coefficient (SC) with frequency typically showed a low-pass characteristic. 3. The capacity of phase-locking to tones was correlated with the functional classification of a DMN neuron and the firing rate of its CF response. Primarylike neurons exhibited various degrees of phase-locked discharges to tones at off-CF frequencies. The average upper cutoff frequency, i.e., the frequency at which the SC dropped to 0.5 of maximum value, differed for the three classes of primarylike neurons. The average cutoff frequency was respectively 183, 325, and 536 Hz for primarylike neurons that displayed low (PL-1), intermediate (PL-2), and high (PL-3) steady-state firing rates to CF stimulation. The phasic neurons showed poor phase-locking capacities at all tone frequencies. 4. The frequency range of phase-locking to amplitude-modulated stimuli was also different for the different cell types, as evidenced by the units' modulation transfer functions (MTFs). The primarylike neurons exhibited mostly all-pass or low-pass sync-based MTFs. The mean upper cutoff frequencies for primarylike neurons having low-pass MTFs were 155 Hz for PL-1 neurons, 176 Hz for PL-2 neurons, and 218 Hz for PL-3 neurons. Pauser, chopper, phasic, and phasic-burst neurons gave mostly low-pass MTFs having a mean upper cutoff frequency of 219, 235, 242, and 251 Hz, respectively. 5. The phase-locking ability of DMN neurons to tones and to amplitude-modulated stimuli are compared with those of frog's primary afferent fibers and with those of avian and mammalian cochlear nucleus neurons. The significance of results in terms of sound localization and sound pattern recognition is discussed.


2007 ◽  
Vol 98 (4) ◽  
pp. 1941-1952 ◽  
Author(s):  
Mark N. Wallace ◽  
Lucy A. Anderson ◽  
Alan R. Palmer

Accurate temporal coding of low-frequency tones by spikes that are locked to a particular phase of the sine wave (phase-locking), occurs among certain groups of neurons at various processing levels in the brain. Phase-locked responses have previously been studied in the inferior colliculus and neocortex of the guinea pig and we now describe the responses in the auditory thalamus. Recordings were made from 241 single units, 32 (13%) of which showed phase-locked responses. Units with phase-locked responses were mainly (82%) located in the ventral division of the medial geniculate body (MGB), and also the medial division (18%), but were not found in the dorsal or shell divisions. The upper limiting frequency of phase-locking varied greatly between units (60–1,100 Hz) and between anatomical divisions. The upper limit in the ventral division was 520 Hz and in the medial was 1,100 Hz. The range of steady-state delays calculated from phase plots also varied: ventral division, 8.6–14 ms (mean 11.1 ms; SD 1.56); medial division, 7.5–11 ms (mean 9.3 ms; SD 1.5). Taken together, these measurements are consistent with the medial division receiving a phase-locked input directly from the brain stem, without an obligatory relay in the inferior colliculus. Cells in both the ventral and medial divisions of the MGB showed a response that phase-locked to the fundamental frequency of a guinea pig purr and may be involved in analyzing communication calls.


1990 ◽  
Vol 63 (5) ◽  
pp. 1169-1190 ◽  
Author(s):  
G. A. Spirou ◽  
W. E. Brownell ◽  
M. Zidanic

1. Recordings were made from single nerve fibers in barbiturate-anesthetized cats in the midline trapezoid body, a location that permits selective sampling of efferent cells of the ventral cochlear nucleus. Single units were localized to either the dorsal or ventral components of the trapezoid body. The fibers were physiologically classified on the basis of their peristimulus time histograms (PSTH) and receptive-field properties. In addition, low characteristic frequency (CF) units were probed for rapid rate and phase shifts with increases in intensity. The projection patterns of some fibers were traced by iontophoresing horseradish peroxidase (HRP) into their axons. 2. HRP-labeled fibers most likely originated from globular bushy cells of the ventral cochlear nucleus in that they sent a large branch into the contralateral medial nucleus of the trapezoid body which terminated in a calyceal ending and an ipsilateral branch into the lateral nucleus of the trapezoid body. A thin branch, usually starting from the large branch, wound its way through the medial nucleus of the trapezoid body to its termination in the ventral nucleus of the trapezoid body. Additional branches from the parent axon could pass through medial periolivary groups throughout the rostrocaudal extent of the superior olivary complex. The parent fiber was traced as far as the ventral lateral lemniscus where it faded before reaching its termination. 3. The majority of units were recorded in the ventral component of the trapezoid body. Although the ventral component is comprised of both large and small diameter fibers, our sample was biased to the larger diameter fibers representing the activity of axons originating from globular bushy cells in the ventral cochlear nucleus. Ventral component units were not tonotopically arrayed and had CFs that spanned the audible range for cats. HRP labeling of ventral component axons revealed that the section of the axon traveling through the midline shifted its dorsal-ventral location. This pattern was compatible with the lack of tonotopy found in the ventral component. Recordings were also made from the dorsal component of the trapezoid body, which contained medium diameter axons. These axons originated from spherical bushy cells in the ventral cochlear nucleus. Dorsal component units were tonotopically arrayed and had CFs less than 7 kHz. 4. Cells were characterized by their PSTH at CF. Primary-like and phase-locked units constituted most of the dorsal component units.(ABSTRACT TRUNCATED AT 400 WORDS)


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