Burst-firing sharpens frequency-tuning in primary auditory cortex

Neuroreport ◽  
1996 ◽  
Vol 7 (3) ◽  
pp. 753-757 ◽  
Author(s):  
Jos J. Eggermont ◽  
Geoff M. Smith
2021 ◽  
Vol 15 ◽  
Author(s):  
Wenlu Pan ◽  
Jing Pan ◽  
Yan Zhao ◽  
Hongzheng Zhang ◽  
Jie Tang

Serotonin transporter (SERT) modulates the level of 5-HT and significantly affects the activity of serotonergic neurons in the central nervous system. The manipulation of SERT has lasting neurobiological and behavioral consequences, including developmental dysfunction, depression, and anxiety. Auditory disorders have been widely reported as the adverse events of these mental diseases. It is unclear how SERT impacts neuronal connections/interactions and what mechanism(s) may elicit the disruption of normal neural network functions in auditory cortex. In the present study, we report on the neuronal morphology and function of auditory cortex in SERT knockout (KO) mice. We show that the dendritic length of the fourth layer (L-IV) pyramidal neurons and the second-to-third layer (L-II/III) interneurons were reduced in the auditory cortex of the SERT KO mice. The number and density of dendritic spines of these neurons were significantly less than those of wild-type neurons. Also, the frequency-tonotopic organization of primary auditory cortex was disrupted in SERT KO mice. The auditory neurons of SERT KO mice exhibited border frequency tuning with high-intensity thresholds. These findings indicate that SERT plays a key role in development and functional maintenance of auditory cortical neurons. Auditory function should be examined when SERT is selected as a target in the treatment for psychiatric disorders.


1999 ◽  
Vol 82 (5) ◽  
pp. 2327-2345 ◽  
Author(s):  
Jagmeet S. Kanwal ◽  
Douglas C. Fitzpatrick ◽  
Nobuo Suga

Mustached bats, Pteronotus parnellii parnellii,emit echolocation pulses that consist of four harmonics with a fundamental consisting of a constant frequency (CF1-4) component followed by a short, frequency-modulated (FM1-4) component. During flight, the pulse fundamental frequency is systematically lowered by an amount proportional to the velocity of the bat relative to the background so that the Doppler-shifted echo CF2 is maintained within a narrowband centered at ∼61 kHz. In the primary auditory cortex, there is an expanded representation of 60.6- to 63.0-kHz frequencies in the “Doppler-shifted CF processing” (DSCF) area where neurons show sharp, level-tolerant frequency tuning. More than 80% of DSCF neurons are facilitated by specific frequency combinations of ∼25 kHz (BFlow) and ∼61 kHz (BFhigh). To examine the role of these neurons for fine frequency discrimination during echolocation, we measured the basic response parameters for facilitation to synthesized echolocation signals varied in frequency, intensity, and in their temporal structure. Excitatory response areas were determined by presenting single CF tones, facilitative curves were obtained by presenting paired CF tones. All neurons showing facilitation exhibit at least two facilitative response areas, one of broad spectral tuning to frequencies centered at BFlowcorresponding to a frequency in the lower half of the echolocation pulse FM1 sweep and another of sharp tuning to frequencies centered at BFhigh corresponding to the CF2 in the echo. Facilitative response areas for BFhigh are broadened by ∼0.38 kHz at both the best amplitude and 50 dB above threshold response and show lower thresholds compared with the single-tone excitatory BFhigh response areas. An increase in the sensitivity of DSCF neurons would lead to target detection from farther away and/or for smaller targets than previously estimated on the basis of single-tone responses to BFhigh. About 15% of DSCF neurons show oblique excitatory and facilitatory response areas at BFhigh so that the center frequency of the frequency-response function at any amplitude decreases with increasing stimulus amplitudes. DSCF neurons also have inhibitory response areas that either skirt or overlap both the excitatory and facilitatory response areas for BFhigh and sometimes for BFlow. Inhibition by a broad range of frequencies contributes to the observed sharpness of frequency tuning in these neurons. Recordings from orthogonal penetrations show that the best frequencies for facilitation as well as excitation do not change within a cortical column. There does not appear to be any systematic representation of facilitation ratios across the cortical surface of the DSCF area.


1998 ◽  
Vol 80 (5) ◽  
pp. 2743-2764 ◽  
Author(s):  
Jos J. Eggermont

Eggermont, Jos J. Representation of spectral and temporal sound features in three cortical fields of the cat. Similarities outweigh differences. J. Neurophysiol. 80: 2743–2764, 1998. This study investigates the degree of similarity of three different auditory cortical areas with respect to the coding of periodic stimuli. Simultaneous single- and multiunit recordings in response to periodic stimuli were made from primary auditory cortex (AI), anterior auditory field (AAF), and secondary auditory cortex (AII) in the cat to addresses the following questions: is there, within each cortical area, a difference in the temporal coding of periodic click trains, amplitude-modulated (AM) noise bursts, and AM tone bursts? Is there a difference in this coding between the three cortical fields? Is the coding based on the temporal modulation transfer function (tMTF) and on the all-order interspike-interval (ISI) histogram the same? Is the perceptual distinction between rhythm and roughness for AM stimuli related to a temporal versus spatial representation of AM frequency in auditory cortex? Are interarea differences in temporal response properties related to differences in frequency tuning? The results showed that: 1) AM stimuli produce much higher best modulation frequencies (BMFs) and limiting rates than periodic click trains. 2) For periodic click trains and AM noise, the BMFs and limiting rates were not significantly different for the three areas. However, for AM tones the BMF and limiting rates were about a factor 2 lower in AAF compared with the other areas. 3) The representation of stimulus periodicity in ISIs resulted in significantly lower mean BMFs and limiting rates compared with those estimated from the tMTFs. The difference was relatively small for periodic click trains but quite large for both AM stimuli, especially in AI and AII. 4) Modulation frequencies <20 Hz were represented in the ISIs, suggesting that rhythm is coded in auditory cortex in temporal fashion. 5) In general only a modest interdependence of spectral- and temporal-response properties in AI and AII was found. The BMFs were correlated positively with characteristic frequency in AAF. The limiting rate was positively correlated with the frequency-tuning curve bandwidth in AI and AII but not in AAF. Only in AAF was a correlation between BMF and minimum latency was found. Thus whereas differences were found in the frequency-tuning curve bandwidth and minimum response latencies among the three areas, the coding of periodic stimuli in these areas was fairly similar with the exception of the very poor representation of AM tones in AII. This suggests a strong parallel processing organization in auditory cortex.


1993 ◽  
Vol 69 (4) ◽  
pp. 1292-1313 ◽  
Author(s):  
J. J. Eggermont ◽  
G. M. Smith ◽  
D. Bowman

1. Neural activity was recorded with two independent electrodes separated by 0.5-2 mm, aligned in parallel, and advanced perpendicular to the surface of the cat auditory cortex. Because the experiments were part of a study into laminar interaction the difference in recording depths for the two independently movable electrodes was never > 100 microns. Multi-unit activity on each electrode was separated on-line into single-unit spike-trains with a maximum variance spike sorting algorithm. Off-line controls on the quality of the spike-train separation were routinely performed. The first aim of this study was to describe the age dependence of spontaneous burst firing and to explore if and how it could be explained by age dependent changes in firing rate. The second aim was to investigate a potential layer dependence on burst firing. The third aim was to describe the effect of burst-removal procedures on the shape, strength, and width of the cross-correlogram and to investigate whether an age dependence in burst firing might account for the previously reported age dependence in correlation strengths. 2. Recordings were made from 237 single units from primary auditory cortex in nine adult cats and from 67 units in seven kittens age 10-52 days. The incidence of burst firing as a function of firing rate, age and depth of recording and unit characteristic frequency was investigated. In addition the effect of burst firing on the strength and width of the central peak in 471 neural pair correlograms was analyzed. 3. Burst firing could be distinguished at many different time scales; bursts lasting of the order of 10 s contained bursts with durations of the order of 1 s, which in turn contained bursts of 30-50-ms duration. The analysis in this paper was restricted to the short-duration bursts. 4. Burst firing on the short-time scale of 50 ms was characterized by relatively well defined intervals between the first two spikes (3-15 ms) followed by higher-order intervals with large spread (range 4-50 ms) but with increasing modal interval value. The typical adult five-spike burst template featured spikes at 0, 3.3, 14.6, 27.2, and 34.8 ms. Burst with fewer spikes showed larger intervals between the first three spikes. 5. The probability of occurrence of isolated spikes, pairs, triplets, etc. showed a power-law dependence on firing rate with a coefficient that was significantly lower than expected under Poisson firing conditions.(ABSTRACT TRUNCATED AT 400 WORDS)


2015 ◽  
Vol 112 (52) ◽  
pp. 16036-16041 ◽  
Author(s):  
Federico De Martino ◽  
Michelle Moerel ◽  
Kamil Ugurbil ◽  
Rainer Goebel ◽  
Essa Yacoub ◽  
...  

Columnar arrangements of neurons with similar preference have been suggested as the fundamental processing units of the cerebral cortex. Within these columnar arrangements, feed-forward information enters at middle cortical layers whereas feedback information arrives at superficial and deep layers. This interplay of feed-forward and feedback processing is at the core of perception and behavior. Here we provide in vivo evidence consistent with a columnar organization of the processing of sound frequency in the human auditory cortex. We measure submillimeter functional responses to sound frequency sweeps at high magnetic fields (7 tesla) and show that frequency preference is stable through cortical depth in primary auditory cortex. Furthermore, we demonstrate that—in this highly columnar cortex—task demands sharpen the frequency tuning in superficial cortical layers more than in middle or deep layers. These findings are pivotal to understanding mechanisms of neural information processing and flow during the active perception of sounds.


2018 ◽  
Author(s):  
Huan-huan Zeng ◽  
Jun-feng Huang ◽  
Ming Chen ◽  
Yun-qing Wen ◽  
Zhi-ming Shen ◽  
...  

AbstractMarmoset has emerged as a useful non-human primate species for studying the brain structure and function. Previous studies on the mouse primary auditory cortex (A1) showed that neurons with preferential frequency tuning responses are mixed within local cortical regions, despite a large-scale tonotopic organization. Here we found that frequency tuning properties of marmoset A1 neurons are highly uniform within local cortical regions. We first defined tonotopic map of A1 using intrinsic optical imaging, and then used in vivo two-photon calcium imaging of large neuronal populations to examine the tonotopic preference at the single-cell level. We found that tuning preferences of layer 2/3 neurons were highly homogeneous over hundreds of micrometers in both horizontal and vertical directions. Thus, marmoset A1 neurons are distributed in a tonotopic manner at both macro- and microscopic levels. Such organization is likely to be important for the organization of auditory circuits in the primate brain.


2011 ◽  
Vol 106 (2) ◽  
pp. 849-859 ◽  
Author(s):  
Edward L. Bartlett ◽  
Srivatsun Sadagopan ◽  
Xiaoqin Wang

The frequency resolution of neurons throughout the ascending auditory pathway is important for understanding how sounds are processed. In many animal studies, the frequency tuning widths are about 1/5th octave wide in auditory nerve fibers and much wider in auditory cortex neurons. Psychophysical studies show that humans are capable of discriminating far finer frequency differences. A recent study suggested that this is perhaps attributable to fine frequency tuning of neurons in human auditory cortex (Bitterman Y, Mukamel R, Malach R, Fried I, Nelken I. Nature 451: 197–201, 2008). We investigated whether such fine frequency tuning was restricted to human auditory cortex by examining the frequency tuning width in the awake common marmoset monkey. We show that 27% of neurons in the primary auditory cortex exhibit frequency tuning that is finer than the typical frequency tuning of the auditory nerve and substantially finer than previously reported cortical data obtained from anesthetized animals. Fine frequency tuning is also present in 76% of neurons of the auditory thalamus in awake marmosets. Frequency tuning was narrower during the sustained response compared to the onset response in auditory cortex neurons but not in thalamic neurons, suggesting that thalamocortical or intracortical dynamics shape time-dependent frequency tuning in cortex. These findings challenge the notion that the fine frequency tuning of auditory cortex is unique to human auditory cortex and that it is a de novo cortical property, suggesting that the broader tuning observed in previous animal studies may arise from the use of anesthesia during physiological recordings or from species differences.


1995 ◽  
Vol 74 (5) ◽  
pp. 1841-1855 ◽  
Author(s):  
D. M. Bowman ◽  
J. J. Eggermont ◽  
G. M. Smith

1. Neural activity was recorded extracellularly with two independent microelectrodes aligned in parallel and advanced perpendicular to isofrequency sheets in cat primary auditory cortex. Multiunit activity was separated into single-unit spike trains using a maximum variance spike sorting algorithm. Only units that demonstrated a high quality of sorting and a minimum spontaneous firing rate of 0.2 spikes/s were considered for analysis. The primary aim of this study was to describe the effect of periodic click train and broadband noise stimulation on short-time-scale (< or = 50 ms) bursts in the spike trains of single auditory cortical units and to determine whether stimulation influenced the occurrence, spike count, and/or temporal structure of burst firing relative to a spontaneous baseline. 2. Extracellular recordings were made in 20 juvenile and adult cats from 69 single auditory cortical units during click train stimulation and silence, and from 30 single units during noise stimulation and in silence. In an additional 15 single units the effect of both click train and noise stimulation was investigated. The incidence, spike count, and temporal structure of short-time-scale burst firing in the first 100 ms following stimulus presentation was compared with burst firing in the period starting 500 ms after stimulus presentation and with spontaneous burst firing. In addition, the serial dependence of interspike intervals within a burst was tested during periods of stimulation. 3. Burst firing was present in the stimulation, poststimulation, and spontaneous conditions. Longer bursts (consisting of > or = 3 spikes) were more commonly observed in the poststimulation and spontaneous conditions than in the stimulation condition. This effect was most pronounced during click stimulation. A period of elevated firing activity was present in a subset of units 0.5-1.5 s after stimulus presentation, indicating prolonged effects of stimulation on single-unit firing behavior. 4. For both stimuli, the proportion of single-unit responses composed of bursts was significantly greater in poststimulation and spontaneous periods than during stimulation. Burst rate was higher in post-click-train stimulation and spontaneous periods than during periods of click stimulation. The isolated spike rate was significantly higher during periods of noise and click stimulation than in the poststimulation and spontaneous periods. 5. An examination of the autocorrelograms and higher-order interspike interval histograms of single-unit responses during click train stimulation indicated that 25% of single-unit spike trains contained an excess of brief first-order intervals and 14% of spike trains contained a shortage of long higher-order interspike intervals relative to a spontaneous baseline. During noise stimulation, 10% of single-unit responses contained an excess of short intervals relative to baseline. Interspike intervals of short-duration bursts were not serially dependent during periods of stimulation. 6. A comparison of the autocorrelograms and higher-order interval histograms of single-unit responses in the poststimulation and spontaneous conditions indicated that 20% of single-unit spike trains contained an excess of short first-, second-, and third-order intervals following stimulation. This subgroups of single units could not be distinguished on the basis of the age of the animal or the depth at which the recording was made. 7. The low incidence of burst firing during stimulation opposes the view that bursts serve as a mechanism to emphasize or amplify particular stimulus-related responses in the presence of ongoing spontaneous activity in the primary auditory cortex. Moreover, there is little evidence to support the notion that brief bursts represent neural codes, because intraburst intervals are not serially dependent. It is suggested that pyramidal burst firing may be an effective way to evoke postsynaptic firing in inhibitory interneurons and subsequ


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