Interaction between excitation and inhibition affects frequency tuning curve, response size and latency of neurons in the auditory cortex of the big brown bat, Eptesicus fuscus

2002 ◽  
Vol 174 (1-2) ◽  
pp. 281-289 ◽  
Author(s):  
Philip H.-S Jen ◽  
Qi Cai Chen ◽  
Fei Jian Wu
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.


2004 ◽  
Vol 92 (6) ◽  
pp. 3192-3199 ◽  
Author(s):  
Xiaofeng Ma ◽  
Nobuo Suga

Repetitive acoustic stimulation, auditory fear conditioning, and focal electric stimulation of the auditory cortex (AC) each evoke the reorganization of the central auditory system. Our current study of the big brown bat indicates that focal electric stimulation of the AC evokes center-surround reorganization of the frequency map of the AC. In the center, the neuron's best frequencies (BFs), together with their frequency–tuning curves, shift toward the BFs of electrically stimulated cortical neurons (centripetal BF shifts). In the surround, BFs shift away from the stimulated cortical BF (centrifugal BF shifts). Centripetal BF shifts are much larger than centrifugal BF shifts. An antagonist (bicuculline methiodide) of inhibitory synaptic transmitter receptors changes centrifugal BF shifts into centripetal BF shifts, whereas its agonist (muscimol) changes centripetal BF shifts into centrifugal BF shifts. This reorganization of the AC thus depends on a balance between facilitation and inhibition evoked by focal cortical electric stimulation. Unlike neurons in the AC of the big brown bat, neurons in the Doppler-shifted constant-frequency (DSCF) area of the AC of the mustached bat are highly specialized for fine-frequency analysis and show almost exclusively centrifugal BF shifts for focal electric stimulation of the DSCF area. Our current data indicate that in the highly specialized area, lateral inhibition is strong compared with the less-specialized area and that the specialized and nonspecialized areas both share the same inhibitory mechanism for centrifugal BF shifts.


2005 ◽  
Vol 93 (1) ◽  
pp. 71-83 ◽  
Author(s):  
Jun Yan ◽  
Yunfeng Zhang ◽  
Günter Ehret

Plasticity of the auditory cortex can be induced by conditioning or focal cortical stimulation. The latter was used here to measure how stimulation in the tonotopy of the mouse primary auditory cortex influences frequency tuning in the midbrain central nucleus of the inferior colliculus (ICC). Shapes of collicular frequency tuning curves (FTCs) were quantified before and after cortical activation by measuring best frequencies, FTC bandwidths at various sound levels, level tolerance, Q-values, steepness of low- and high-frequency slopes, and asymmetries. We show here that all of these measures were significantly changed by focal cortical activation. The changes were dependent not only on the relationship of physiological properties between the stimulated cortical neurons and recorded collicular neurons but also on the tuning curve class of the collicular neuron. Cortical activation assimilated collicular FTC shapes; sharp and broad FTCs were changed to the shapes comparable to those of auditory nerve fibers. Plasticity in the ICC was organized in a center (excitatory)-surround (inhibitory) way with regard to the stimulated location (i.e., the frequency) of cortical tonotopy. This ensures, together with the spatial gradients of distribution of collicular FTC shapes, a sharp spectral filtering at the core of collicular frequency-band laminae and an increase in frequency selectivity at the periphery of the laminae. Mechanisms of FTC plasticity were suggested to comprise both corticofugal and local ICC components of excitatory and inhibitory modulation leading to a temporary change of the balance between excitation and inhibition in the ICC.


2000 ◽  
Vol 83 (4) ◽  
pp. 1856-1863 ◽  
Author(s):  
Syed A. Chowdhury ◽  
Nobuo Suga

In a search phase of echolocation, big brown bats, Eptesicus fuscus, emit biosonar pulses at a rate of 10/s and listen to echoes. When a short acoustic stimulus was repetitively delivered at this rate, the reorganization of the frequency map of the primary auditory cortex took place at and around the neurons tuned to the frequency of the acoustic stimulus. Such reorganization became larger when the acoustic stimulus was paired with electrical stimulation of the cortical neurons tuned to the frequency of the acoustic stimulus. This reorganization was mainly due to the decrease in the best frequencies of the neurons that had best frequencies slightly higher than those of the electrically stimulated cortical neurons or the frequency of the acoustic stimulus. Neurons with best frequencies slightly lower than those of the acoustically and/or electrically stimulated neurons slightly increased their best frequencies. These changes resulted in the over-representation of repetitively delivered acoustic stimulus. Because the over-representation resulted in under-representation of other frequencies, the changes increased the contrast of the neural representation of the acoustic stimulus. Best frequency shifts for over-representation were associated with sharpening of frequency-tuning curves of 25% of the neurons studied. Because of the increases in both the contrast of neural representation and the sharpness of tuning, the over-representation of the acoustic stimulus is accompanied with an improvement of analysis of the acoustic stimulus.


1997 ◽  
Vol 77 (5) ◽  
pp. 2360-2372 ◽  
Author(s):  
Daphna Ehrlich ◽  
John H. Casseday ◽  
Ellen Covey

Ehrlich, Daphna, John H. Casseday, and Ellen Covey. Neural tuning to sound duration in the inferior colliculus of the big brown bat, Eptesicus fuscus. J. Neurophysiol. 77: 2360–2372, 1997. Neural tuning to different sound durations may be a useful filter for identification of certain sounds, especially those that are biologically important. The auditory midbrains of mammals and amphibians contain neurons that appear to be tuned to sound duration. In amphibians, neurons are tuned to durations of sound that are biologically important. The purpose of this study was to characterize responses of neurons in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus, to sounds of different durations. Our aims were to determine what percent of neurons are duration tuned and how best durations are correlated to durations of echolocation calls, and to examine response properties that may be relevant to the mechanism for duration tuning, such as latency and temporal firing pattern; we also examined frequency tuning and rate-level functions. We recorded from 136 single units in the central nucleus of the IC of unanesthetized bats. The stimuli were pure tones, frequency-modulated sweeps, and broadband noise. The criterion for duration tuning was an increase in spike count of ≥50% at some durations compared with others. Of the total units sampled, 36% were tuned to stimulus duration. All of these units were located in the caudal half of the IC. Best duration for most units ranged from <1 to 10 ms, but a few had best durations up to ≥20 ms. This range is similar to the range of durations of echolocation calls used by Eptesicus. All duration-tuned neurons responded transiently. The minimum latency was always longer than the best duration. Duration-tuned units have best durations and best frequencies that match the temporal structure and frequency range of the echolocation calls. Thus the results raise the hypothesis that neurons in the IC of Eptesicus, and probably the auditory midbrain of other vertebrates, are tuned to biologically important sound durations. We suggest a model for duration tuning consisting of three components: 1) inhibitory input that is correlated with the onset of the stimulus and is sustained for the stimulus duration; 2) transient excitation that is correlated with the offset of the stimulus; and 3) transient excitation that is correlated with the onset of the stimulus but is delayed in time relative to the onset of inhibition. For the neuron to fire, the two excitatory events must coincide in time; noncoincident excitatory events are not sufficient.


1984 ◽  
Vol 51 (1) ◽  
pp. 147-163 ◽  
Author(s):  
D. P. Phillips ◽  
S. S. Orman

In the auditory cortex of barbiturate-anesthetized cats, the posterior auditory field (field P) was identified by its tonotopic organization, and single neurons in that field were studied quantitatively for their sensitivity to the frequency and intensity of tonal stimuli presented via calibrated, sealed stimulating systems. Field P neurons had narrow, V-shaped, threshold frequency tuning curves. At suprathreshold levels, spike counts were generally greatest at frequencies at or close to the neuron's threshold best frequency (BF). Eighty-six percent of posterior-field neurons displayed spike counts that were a nonmonotonic function of the intensity of a BF tone. Of these, over 90% showed at least a 50% reduction in spike count at high stimulus levels, and almost 20% of nonmonotonic cells ceased responding entirely at high stimulus intensities. The nonmonotonic shape of spike count-versus-intensity profiles was typically preserved across the range of frequencies to which any given neuron was responsive. For some neurons, this had the consequence of generating a completely circumscribed frequency-intensity response area. That is, these neurons responded to a tonal stimulus only if the stimulus was within a restricted range of both frequency and intensity. These response areas showed internal organizations that appeared to reflect one or both of two processes. For some neurons, the optimal sound pressure level for spike counts varied with tone frequency, roughly paralleling the threshold tuning curve. For other neurons, the optimal sound pressure level tended to be constant across frequency despite threshold variations of up to 20 dB. The minimum response latencies of posterior-field neurons were generally in the range of 20-50 ms, while cells in the primary auditory cortex (AI) in the same animals generally had minimum latent periods of less than 20 ms. Comparison of these data with those previously presented for neurons in two other cortical auditory fields suggests that the cat's auditory cortex might show an interfield segregation of neurons according to their coding properties.


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