Monaural inhibition in cat auditory cortex

1995 ◽  
Vol 73 (5) ◽  
pp. 1876-1891 ◽  
Author(s):  
M. B. Calford ◽  
M. N. Semple
Keyword(s):  
Auditory Cortex ◽  
Lateral Inhibition ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Inhibitory Response ◽  
Forward Masking ◽  
Excitatory Response ◽  
Rate Level ◽  
Wide Range ◽  
Response Area

1. Several studies of auditory cortex have examined the competitive inhibition that can occur when appropriate sounds are presented to each ear. However, most cortical neurons also show both excitation and inhibition in response to presentation of stimuli at one ear alone. The extent of such inhibition has not been described. Forward masking, in which a variable masking stimulus was followed by a fixed probe stimulus (within the excitatory response area), was used to examine the extent of monaural inhibition for neurons in primary auditory cortex of anesthetized cats (barbiturate or barbiturate-ketamine). Both the masking and probe stimuli were 50-ms tone pips presented to the contralateral ear. Most cortical neurons showed significant forward masking at delays beyond which masking effects in the auditory nerve are relatively small compared with those seen in cortical neurons. Analysis was primarily concerned with such components. Standard rate-level functions were also obtained and were examined for nonmonotonicity, an indication of level-dependent monaural inhibition. 2. Consistent with previous reports, a wide range of frequency tuning properties (excitatory response area shapes) was found in cortical neurons. This was matched by a wide range of forward-masking-derived inhibitory response areas. At the most basic level of analysis, these were classified according to the presence of lateral inhibition, i.e., where a probe tone at a neuron's characteristic frequency was masked by tones outside the limits of the excitatory response area. Lateral inhibition was a property of 38% of the sampled neurons. Such neurons represented 77% of those with nonmonotonic rate-level functions, indicating a strong correlation between the two indexes of monaural inhibition; however, the shapes of forward masking inhibitory response areas did not usually correspond with those required to account for the "tuning" of a neuron. In addition, it was found that level-dependent inhibition was not added to by forward masking inhibition. 3. Analysis of the discharges to individual stimulus pair presentations, under conditions of partial masking, revealed that discharges to the probe occurred independently of discharges to the preceding masker. This indicates that even when the masker is within a neuron's excitatory response area, forward masking is not a postdischarge habituation phenomenon. However, for most neurons the degree of masking summed over multiple stimulus presentations appears determined by the same stimulus parameters that determine the probability of response to the masker.(ABSTRACT TRUNCATED AT 400 WORDS)

Lateral Inhibition for Center-Surround Reorganization of the Frequency Map of Bat Auditory Cortex

2004 ◽  
Vol 92 (6) ◽  
pp. 3192-3199 ◽  
Author(s):  
Xiaofeng Ma ◽  
Nobuo Suga
Keyword(s):  
Auditory Cortex ◽  
Lateral Inhibition ◽  
Cortical Neurons ◽  
Electric Stimulation ◽  
Frequency Tuning ◽  
Constant Frequency ◽  
Specialized Area ◽  
Big Brown Bat ◽  
Frequency Map ◽  
Stimulation Of

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.

scholarly journals Serotonin Transporter Defect Disturbs Structure and Function of the Auditory Cortex in Mice

2021 ◽  
Vol 15 ◽  
Author(s):  
Wenlu Pan ◽  
Jing Pan ◽  
Yan Zhao ◽  
Hongzheng Zhang ◽  
Jie Tang
Keyword(s):  
Auditory Cortex ◽  
Serotonin Transporter ◽  
Cortical Neurons ◽  
Pyramidal Neurons ◽  
Frequency Tuning ◽  
Primary Auditory Cortex ◽  
Neuronal Morphology ◽  
Neuronal Connections ◽  
The Central Nervous System ◽  
And Function

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.

scholarly journals Facilitatory and Inhibitory Frequency Tuning of Combination-Sensitive Neurons in the Primary Auditory Cortex of Mustached Bats

1999 ◽  
Vol 82 (5) ◽  
pp. 2327-2345 ◽  
Author(s):  
Jagmeet S. Kanwal ◽  
Douglas C. Fitzpatrick ◽  
Nobuo Suga
Keyword(s):  
Auditory Cortex ◽  
Frequency Tuning ◽  
Temporal Structure ◽  
Primary Auditory Cortex ◽  
Frequency Discrimination ◽  
Inhibitory Response ◽  
Center Frequency ◽  
Constant Frequency ◽  
Single Tone ◽  
Threshold Response

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.

Effect of tone-pulse rise time on rate-level functions of cat auditory cortex neurons: excitatory and inhibitory processes shaping responses to tone onset

1988 ◽  
Vol 59 (5) ◽  
pp. 1524-1539 ◽  
Author(s):  
D. P. Phillips
Keyword(s):  
Auditory Cortex ◽  
Rise Time ◽  
Cortical Neurons ◽  
Tone Onset ◽  
Tone Frequency ◽  
Pulse Envelope ◽  
Pulse Rise Time ◽  
Rate Level ◽  
Tone Pulse ◽  
Level Function

1. The responses of cat auditory cortex neurons are largely dominated by transient stimulus events, including tone-pulse onset. In addition, these neurons often receive sensitive inhibitory inputs in tone frequency-intensity domains flanking the excitatory one centered at characteristic frequency (CF). These observations suggest that auditory cortex neurons might be sensitive to the spectral splatter that occurs at tone onset due to the tone-pulse envelope shape. 2. To investigate this hypothesis, single neurons in the primary auditory cortex of anesthetized cats were studied for the form of their spike-rate versus tone-level functions using CF tone pulses of different rise times. Stimuli were presented to the contralateral ear using a calibrated, sealed stimulus delivery system. 3. Some neurons with monotonic rate-level functions for conventional (5-10 ms) rise-time tones were relatively insensitive to variations in tone-pulse rise time. Other monotonic neurons showed rate-level functions that became increasingly bell shaped for shorter rise-time stimuli. All neurons with bell-shaped, nonmonotonic rate-level functions for conventional rise-time tones became increasingly nonmonotonic for shorter rise-time signals. In the same neurons, lengthening of tone rise times typically reduced the slope of the high-intensity, descending limb of the rate-level function, in some cases to zero. 4. This pattern of rise-time effects is consistent with previous evidence on the association between rate-level function shape and the presence of inhibitory tone response areas flanking the excitatory one at CF. The present data suggest that cortical neurons are sensitive to the gross shape of the short-term stimulus spectrum at tone onset, and that for many neurons, the nonmonotonic form of CF tone rate level functions may be configured as much by the rate of tone onset as by the plateau amplitude of a tone pulse.

Noradrenergic Induction of Selective Plasticity in the Frequency Tuning of Auditory Cortex Neurons

2004 ◽  
Vol 92 (3) ◽  
pp. 1445-1463 ◽  
Author(s):  
Yves Manunta ◽  
Jean-Marc Edeline
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Cortical Plasticity ◽  
Frequency Tuning ◽  
Tone Frequency ◽  
Cortical Cells ◽  
Tuning Curves ◽  
Alpha Receptors ◽  
Frequency Changes ◽  
Selective Effects

Neuromodulators have long been viewed as permissive factors in experience-induced cortical plasticity, both during development and in adulthood. Experiments performed over the last two decades have reported the potency of acetylcholine to promote changes in functional properties of cortical cells in the auditory, visual, and somatosensory modality. In contrast, very few attempts were made with the monoaminergic systems. The present study evaluates how repeated presentation of brief pulses of noradrenaline (NA) concomitant with presentation of a particular tone frequency changes the frequency tuning curves of auditory cortex neurons determined at 20 dB above threshold. After 100 trials of NA-tone pairing, 28% of the cells (19/67) exhibited selective tuning modifications for the frequency paired with NA. All the selective effects were obtained when the paired frequency was within 1/4 of an octave from the initial best frequency. For these cells, selective decreases were prominent (15/19 cases), and these effects lasted ≥15 min after pairing. No selective effects were observed under various control conditions: tone alone ( n = 10 cells), NA alone ( n = 11 cells), pairing with ascorbic acid ( n = 6 cells), or with GABA ( n = 20 cells). Selective effects were observed when the NA-tone pairing was performed in the presence of propranolol (4/10 cells) but not when it was performed in the presence phentolamine (0/13 cells), suggesting that the effects were mediated by alpha receptors. These results indicate that brief increases in noradrenaline concentration can trigger selective modifications in the tuning curves of cortical neurons that, in most of the cases, go in opposite direction compared with those usually reported with acetylcholine.

Temporal-frequency tuning of cross-orientation suppression in the cat striate cortex

2001 ◽  
Vol 18 (6) ◽  
pp. 941-948 ◽  
Author(s):  
JOHN D. ALLISON ◽  
KEVIN R. SMITH ◽  
A.B. BONDS
Keyword(s):  
Cortical Neurons ◽  
Striate Cortex ◽  
Frequency Tuning ◽  
Temporal Frequency ◽  
Cutoff Frequency ◽  
Excitatory Response ◽  
Temporal Properties ◽  
Low Pass ◽  
Orientation Domain ◽  
Spatial And Temporal Characteristics

A sinusoidal mask grating oriented orthogonally to and superimposed onto an optimally oriented base grating reduces a cortical neuron's response amplitude. The spatial selectivity of cross-orientation suppression (XOR) has been described, so for this paper we investigated the temporal properties of XOR. We recorded from single striate cortical neurons (n = 72) in anesthetized and paralyzed cats. After quantifying the spatial and temporal characteristics of each cell's excitatory response to a base grating, we measured the temporal-frequency tuning of XOR by systematically varying the temporal frequency of a mask grating placed at a null orientation outside of the cell's excitatory orientation domain. The average preferred temporal frequency of the excitatory response of the neurons in our sample was 3.8 (± 1.5 S.D.) Hz. The average cutoff frequency for the sample was 16.3 (± 1.7) Hz. The average preferred temporal frequency (7.0 ± 2.6 Hz) and cutoff frequency (20.4 ± 6.9 Hz) of the XOR were significantly higher. The differences averaged 1.1 (± 0.6) octaves for the peaks and 0.3 (± 0.4) octaves for the cutoffs. The XOR mechanism's preference for high temporal frequencies suggests a possible extrastriate origin for the effect and could help explain the low-pass temporal-frequency response profile displayed by most striate cortical neurons.

scholarly journals Temporal Modulation Transfer Functions in Cat Primary Auditory Cortex: Separating Stimulus Effects From Neural Mechanisms

2002 ◽  
Vol 87 (1) ◽  
pp. 305-321 ◽  
Author(s):  
Jos J. Eggermont
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Transfer Functions ◽  
Frequency Tuning ◽  
Primary Auditory Cortex ◽  
Modulation Transfer ◽  
Temporal Modulation ◽  
Pass Filter ◽  
Low Pass Filter ◽  
Low Pass

We present here a comparison between the local field potentials (LFP) and multiunit (MU) responses, comprising 401 single units, in primary auditory cortex (AI) of 31 cats to periodic click trains, gamma-tone and time-reversed gamma-tone trains, AM noise, AM tones, and frequency-modulated (FM) tones. In a large number of cases, the response to all six stimuli was obtained for the same neurons. We investigate whether cortical neurons are likely to respond to all types of repetitive transients and modulated stimuli and whether a dependence on modulating waveform, or tone or noise carrier, exists. In 97% of the recordings, a temporal modulation transfer function (tMTF) for MU activity was obtained for gamma-tone trains, in 92% for periodic click trains, in 83% for time-reversed gamma-tone trains, in 82% for AM noise, in 71% for FM tones, and only in 53% for AM tones. In 31% of the cases, the units responded to all six stimuli in an envelope-following way. These particular units had significantly larger onset responses to each stimulus compared with all other units. The overall response distribution shows the preference of AI units for stimuli with short rise times such as clicks and gamma tones. It also shows a clear asymmetry in the ability to respond to AM noise and AM tones and points to a strong effect of the frequency content of the carrier on the subcortical processing of AM stimuli. Yet all temporal response properties were independent of characteristic frequency and frequency-tuning curve bandwidth. We show that the observed differences in the tMTFs for different stimuli are to a large extent produced by the different degree of phase locking of the neuronal firings to the envelope of the first stimulus in the train or first modulation period. A normalization procedure, based on these synchronization differences, unified the tMTFs for all stimuli except clicks and allowed the identification of a largely stimulus-invariant, low-pass temporal filter function that most likely reflects the properties of synaptic depression and facilitation. For nonclick stimuli, the low-pass filter has a cutoff frequency of ∼10 Hz and a slope of ∼6 dB/octave. For nonclick stimuli, there was a systematic difference between the vector strength for LFPs and MU activity that can likely be attributed to postactivation suppression mechanisms.

Spatial Organization of Frequency Response Areas and Rate/Level Functions in the Developing AI

2004 ◽  
Vol 91 (2) ◽  
pp. 841-854 ◽  
Author(s):  
Ben H. Bonham ◽  
Steven W. Cheung ◽  
Benoit Godey ◽  
Christoph E. Schreiner
Keyword(s):  
Cortical Neurons ◽  
Spatial Organization ◽  
Frequency Tuning ◽  
Primary Auditory Cortex ◽  
Two Dimensions ◽  
Cortical Region ◽  
Response Properties ◽  
Rate Level ◽  
Bandwidth Tuning ◽  
Adult Cats

The current study was conducted to extend our understanding of changes in spatial organization and response properties of cortical neurons in the developing mammalian forebrain. Extracellular multiunit responses to tones were recorded from a dense array of penetrations covering entire isofrequency contours in the primary auditory cortex (AI) of pentobarbital anesthetized kittens. Ages ranged from postnatal day 14 (P14), shortly after acquisition of normal auditory response thresholds, through postnatal day 111 (P111), when the kittens were largely mature. Spatial organization of the AI was tonotopically ordered by P14. The tonotopic gradient decreased with chronological maturation. At P14 the gradient was about 3.5 kHz/mm. By P111 it had declined to about 2.5 kHz/mm, so that the cortical region encompassing a fixed 3- to 15-kHz frequency range enlarged along its posterior-anterior dimension. Response properties of developing AI neurons changed in both frequency selectivity and intensity selectivity. The mean frequency tuning bandwidth increased with age. Initially, tuning bandwidths were narrow throughout the entire AI. With progressive maturation, broader bandwidths were observed in areas dorsal and ventral to a central region in which neurons remained narrowly tuned. The resulting spatial organization of tuning bandwidth was similar to that reported in adult cats. The majority of recording sites manifested nonmonotonic rate/level functions at all ages. However, the proportion of sites with monotonic rate/level functions increased with age. No spatial organization of rate/level functions (monotonic and nonmonotonic) was observed through P111. The relatively late development of bandwidth tuning in the AI compared with the early presence of tonotopic organization suggests that different developmental processes are responsible for structuring these two dimensions of acoustic selectivity.

Temporally precise population coding of dynamic sounds by auditory cortex

2021 ◽  
Author(s):  
Joshua D Downer ◽  
James Bigelow ◽  
Melissa Runfeldt ◽  
Brian James Malone
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Average Rate ◽  
Relative Effectiveness ◽  
Primary Auditory Cortex ◽  
Population Based ◽  
Population Coding ◽  
Complex Sounds ◽  
Animal Vocalizations

Fluctuations in the amplitude envelope of complex sounds provide critical cues for hearing, particularly for speech and animal vocalizations. Responses to amplitude modulation (AM) in the ascending auditory pathway have chiefly been described for single neurons. How neural populations might collectively encode and represent information about AM remains poorly characterized, even in primary auditory cortex (A1). We modeled population responses to AM based on data recorded from A1 neurons in awake squirrel monkeys and evaluated how accurately single trial responses to modulation frequencies from 4 to 512 Hz could be decoded as functions of population size, composition, and correlation structure. We found that a population-based decoding model that simulated convergent, equally weighted inputs was highly accurate and remarkably robust to the inclusion of neurons that were individually poor decoders. By contrast, average rate codes based on convergence performed poorly; effective decoding using average rates was only possible when the responses of individual neurons were segregated, as in classical population decoding models using labeled lines. The relative effectiveness of dynamic rate coding in auditory cortex was explained by shared modulation phase preferences among cortical neurons, despite heterogeneity in rate-based modulation frequency tuning. Our results indicate significant population-based synchrony in primary auditory cortex and suggest that robust population coding of the sound envelope information present in animal vocalizations and speech can be reliably achieved even with indiscriminate pooling of cortical responses. These findings highlight the importance of firing rate dynamics in population-based sensory coding.

scholarly journals Network Architecture, Receptive Fields, and Neuromodulation: Computational and Functional Implications of Cholinergic Modulation in Primary Auditory Cortex

2006 ◽  
Vol 96 (6) ◽  
pp. 2972-2983 ◽  
Author(s):  
Gabriel Soto ◽  
Nancy Kopell ◽  
Kamal Sen
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Network Architecture ◽  
Frequency Tuning ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Physiological Data ◽  
Cholinergic Modulation ◽  
Tuning Curves ◽  
Intracortical Circuits

Two fundamental issues in auditory cortical processing are the relative importance of thalamocortical versus intracortical circuits in shaping response properties in primary auditory cortex (ACx), and how the effects of neuromodulators on these circuits affect dynamic changes in network and receptive field properties that enhance signal processing and adaptive behavior. To investigate these issues, we developed a computational model of layers III and IV (LIII/IV) of AI, constrained by anatomical and physiological data. We focus on how the local and global cortical architecture shape receptive fields (RFs) of cortical cells and on how different well-established cholinergic effects on the cortical network reshape frequency-tuning properties of cells in ACx. We identify key thalamocortical and intracortical circuits that strongly affect tuning curves of model cortical neurons and are also sensitive to cholinergic modulation. We then study how differential cholinergic modulation of network parameters change the tuning properties of our model cells and propose two different mechanisms: one intracortical (involving muscarinic receptors) and one thalamocortical (involving nicotinic receptors), which may be involved in rapid plasticity in ACx, as recently reported in a study by Fritz and coworkers.

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