Directionality Derived From Differential Sensitivity to Monaural and Binaural Cues in the Cat's Medial Geniculate Body

2000 ◽  
Vol 84 (3) ◽  
pp. 1330-1345 ◽  
Author(s):  
Frank K. Samson ◽  
Pascal Barone ◽  
W. Andrew Irons ◽  
Janine C. Clarey ◽  
Pierre Poirier ◽  
...  
Keyword(s):  
Single Unit ◽  
Medial Geniculate Body ◽  
Broadband Noise ◽  
Differential Sensitivity ◽  
Lateral Part ◽  
Spectral Cues ◽  
Posterior Group ◽  
Monaural Stimulation ◽  
Medial Geniculate ◽  
Monaural Spectral Cues

Azimuth tuning of high-frequency neurons in the primary auditory cortex (AI) is known to depend on binaural disparity and monaural spectral (pinna) cues present in broadband noise bursts. Single-unit response patterns differ according to binaural interactions, strength of monaural excitatory input from each ear, and azimuth sensitivity to monaural stimulation. The latter characteristic has been used as a gauge of neural sensitivity to monaural spectral directional cues. Azimuth sensitivity may depend predominantly on binaural disparity cues, exclusively on monaural spectral cues, or on both. The primary goal of this study was to determine whether each cortical response pattern corresponds to a similar pattern in the medial geniculate body (MGB) or whether some patterns are unique to the cortex. Single-unit responses were recorded from the ventral nucleus (Vn) and lateral part of the posterior group of thalamic nuclei (Po), tonotopic subdivisions of the MGB. Responses to free-field presentation of noise bursts that varied in azimuth and sound pressure level were obtained using methods identical to those used previously in field AI. Many units were azimuth sensitive, i.e., they responded well at some azimuths, and poorly, if at all, at others. These were studied further by obtaining responses to monaural noise stimulation, approximated by reversible plugging of one ear. Monaural directional (MD) cells were sensitive to the azimuth of monaural noise stimulation, whereas binaural directional (BD) cells were either insensitive to its azimuth or monaurally unresponsive. Thus BD and MD cells show differential sensitivity to monaural spectral cues. Monaural azimuth sensitivity could not be used to interpret the spectral sensitivity of predominantly binaural cells that exhibited strong binaural facilitation because they were either unresponsive or poorly responsive to monaural stimulation. The available evidence suggests that some such cells are sensitive to spectral cues. The results do not indicate the presence of any response types in AI that are not present in the MGB. Vn and Po contain similar classes of MD and BD cells. Because Po neurons project to the anterior auditory field, neurons in this cortical area also are likely to exhibit differential sensitivity to binaural disparity and monaural spectral cues. Comparison of these MGB data with a published report of cochlear nucleus (CN) single-unit azimuth tuning shows that MGB sensitivity to spectral cues is considerably stronger than CN sensitivity.

Cortical synthesis of azimuth-sensitive single-unit responses with nonmonotonic level tuning: a thalamocortical comparison in the cat

1996 ◽  
Vol 75 (3) ◽  
pp. 1206-1220 ◽  
Author(s):  
P. Barone ◽  
J. C. Clarey ◽  
W. A. Irons ◽  
T. J. Imig
Keyword(s):  
Single Unit ◽  
Medial Geniculate Body ◽  
Primary Auditory Cortex ◽  
Lateral Part ◽  
Thalamic Nuclei ◽  
Response Properties ◽  
Posterior Group ◽  
Level Function ◽  
Medial Geniculate ◽  
Stimulus Features

1. Azimuth and sound pressure level (SPL) tuning to noise stimulation was characterized in single-unit samples obtained from primary auditory cortex (AI) and in areas of the medial geniculate body (MGB) that project to AI. The primary aim of the study was to test the hypothesis that AI is an important site of synthesis of single-unit responses that exhibit both azimuth sensitivity (tendency for directionally restricted responsiveness) and nonmonotonic (NM) level tuning (tendency for decreased responsiveness with increasing SPL). This was accomplished by comparing the proportions of such responses in AI and MGB. 2. Samples consisted of high-best-frequency (BF) single units located in MGB (n = 217) and AI (n = 216) of barbiturate-anesthetized cats. The MGB sample was obtained mainly from recording sites located in two nuclei that project to AI, the ventral nucleus (VN, n = 118) and the lateral part of the posterior group of thalamic nuclei (Po, n = 84). In addition, a few MGB units were obtained from the medial division (n = 8) or uncertain locations (n = 7). Each unit's responses were studied using noise bursts presented from azimuthal sound directions distributed throughout 180 degrees of the frontal hemifield at 0 degrees elevation. SPL was varied over an 80-dB range in steps of < or = 20 dB at each location. Similarities and differences in azimuth and level tuning were evaluated statistically by comparing the AI sample with the entire MGB sample. If they were found to differ, the AI, VN, and Po samples were compared. 3. Azimuth function modulation was used as a measure of azimuth sensitivity, and its mean was greater in AI than in MGB. NM strength was defined as the percentage reduction in level function value at 75 dB SPL and its mean was greater in AI (showing a greater tendency for decreased responsiveness) than in MGB. Azimuth-sensitive (AS) NM units were identified by jointly categorizing each sample according to both azimuth sensitivity (sensitive and insensitive categories) and NM strength (NM and monotonic categories). AS NM units were much more common in the AI sample than in any of the MGB samples, suggesting that some such responses are synthesized in AI. 4. A vast majority of AI NM units have been reported to be AS, showing a preferential association (linkage) between these two response properties. This finding was confirmed in AI, but was not found to be the case in MGB. This suggests that a linkage between these response properties emerges in the cortex, presumably as a result of synthesis of NM AS responses. Although the functional significance of the linkage is unknown, NM responses may reflect excitatory/inhibitory antagonism that provides AS AI neurons with sensitivity to stimulus features beyond that which is present in MGB. 5. Breadth of azimuth tuning of AS cells was measured as the portion of the frontal hemifield over which azimuth function values were > 75% of maximum (preferred azimuth range, PAR). PARs were broadly distributed in each structure, and mean PAR was narrower in AI than in MGB. A preferred level range (PLR) was defined for NM level functions as the range over which values were > 75% of maximum, and mean PLRs were similar in each sample. There was a weak, but significant, positive correlation between PARs and PLRs in AI but not in MGB. This further suggests a linkage between azimuth and level tuning in AI that does not exist in MGB. 6. Best azimuth (midpoint of the PAR) was used to classify cells as contralateral preferring, ipsilateral preferring, midline preferring, or multipeaked. Samples from AI and MGB exhibited similar distributions of these categories. Contralateral-preferring cells represented a majority of each sample, whereass midline-preferring, ipsilateral-preferring, and multipeaked cells each represented smaller proportions. This suggests that the azimuth preference distribution in AI largely reflects that in MGB. 7. A best SPL was defined as the midpoint of the PLR. This wa

Effects of ear plugging on single-unit azimuth sensitivity in cat primary auditory cortex. II. Azimuth tuning dependent upon binaural stimulation

1994 ◽  
Vol 71 (6) ◽  
pp. 2194-2216 ◽  
Author(s):  
F. K. Samson ◽  
P. Barone ◽  
J. C. Clarey ◽  
T. J. Imig
Keyword(s):  
Auditory Cortex ◽  
Single Unit ◽  
Free Field ◽  
Primary Auditory Cortex ◽  
Excitatory Input ◽  
Spectral Cues ◽  
Binaural Stimulation ◽  
Monaural Stimulation ◽  
Monaural Spectral Cues ◽  
Interaural Level Differences

1. Single-unit recordings were carried out in primary auditory cortex (AI) of barbiturate-anesthetized cats. Observations were based on a sample of 131 high-best-frequency (> 5 kHz), azimuth-sensitive neurons. These were identified by their responses to a set of noise bursts, presented in the free field, that varied in azimuth and sound-pressure level (SPL). Each azimuth-sensitive neuron responded well to some levels at certain azimuths, but did not respond well to any level at other azimuths. 2. Unilateral ear plugging was used to infer each neuron's response to monaural stimulation. Ear plugs, produced by injecting a plastic ear mold compound into the external ear, attenuated sound reaching the tympanic membrane by 25–70 dB. The azimuth tuning of a large proportion of the sample (62/131), referred to as binaural directional (BD), was completely dependent upon binaural stimulation because with one ear plugged, these cells were insensitive to azimuth (either responded well at all azimuths or failed to respond at any azimuth) or in a few cases exhibited striking changes in location of azimuth function peaks. This report describes patterns of monaural responses and binaural interactions exhibited by BD neurons and relates them to each cell's azimuth and level tuning. The response of BD cells to ear plugging is consistent with the hypothesis that they derive azimuth tuning from interaural level differences present in noise bursts. Another component of the sample consisted of monaural directional (27/131) cells that derived azimuth tuning in part or entirely from monaural spectral cues. Cells in the remaining portion of the sample (42/131) responded too unreliably to permit specific conclusions. 3. Binaural interactions were inferred by statistical comparison of a cell's responses to monaural (unilateral plug) and binaural (no plug) stimulation. A larger binaural response than either monaural response was taken as evidence for binaural facilitation. A smaller binaural than monaural response was taken as evidence for binaural inhibition. Binaural facilitation was exhibited by 65% (40/62) of the BD sample (facilitatory cells). Many of these exhibited mixed interactions, i.e., binaural facilitation occurred in response to some azimuth-level combinations, and binaural inhibition to others. Binaural inhibition in the absence of binaural facilitation occurred in 35% (22/62) of the BD sample, a majority of which were EI cells, so called because they received excitatory (E) input from one ear (excitatory ear) and inhibitory (I) input from the other (inhibitory ear). One cell that exhibited binaural inhibition received excitatory input from each ear.(ABSTRACT TRUNCATED AT 400 WORDS)

Intensity functions of single unit responses to tone in the medial geniculate body of cat

1983 ◽  
Vol 11 (2) ◽  
pp. 235-247 ◽  
Author(s):  
E. Rouiller ◽  
Y. de Ribaupierre ◽  
A. Morel ◽  
F. de Ribaupierre
Keyword(s):  
Single Unit ◽  
Medial Geniculate Body ◽  
Medial Geniculate ◽  
Intensity Functions

Monaural Spectral Contrast Mechanism for Neural Sensitivity to Sound Direction in the Medial Geniculate Body of the Cat

1997 ◽  
Vol 78 (5) ◽  
pp. 2754-2771 ◽  
Author(s):  
Thomas J. Imig ◽  
Pierre Poirier ◽  
W. Andrew Irons ◽  
Frank K. Samson
Keyword(s):  
Sound Pressure ◽  
Medial Geniculate Body ◽  
Broadband Noise ◽  
Directional Sensitivity ◽  
Spectral Contrast ◽  
Sound Direction ◽  
Frequency Domains ◽  
Contrast Mechanism ◽  
Medial Geniculate ◽  
Frequency Components

Imig, Thomas J., Pierre Poirier, W. Andrew Irons, and Frank K. Samson. Monaural spectral contrast mechanism for neural sensitivity to sound direction in the medial geniculate body of the cat. J. Neurophysiol. 78: 2754–2771, 1997. Central auditory neurons vary in sound direction sensitivity. Insensitive cells discharge well to all sound source directions, whereas sensitive cells discharge well to certain directions and poorly to others. High-frequency neurons in the latter group are differentially sensitive to binaural and monaural directional cues present in broadband noise (BBN). Binaural directional (BD) cells require binaural stimulation for directional sensitivity; monaural directional (MD) cells are sensitive to the direction of monaural stimuli. A model of MD sensitivity was tested using single-unit responses. The model assumes that MD cells derive directional sensitivity from pinna-derived spectral cues (head related transfer function, HRTF). This assumption was supported by the similarity of effects that pinna orientation produces on locations of HRTF patterns and on locations of MD cell azimuth function peaks and nulls. According to the model, MD neurons derive directional sensitivity by use of excitatory/inhibitory antagonism to compare sound pressure in excitatory and inhibitory frequency domains, and a variety of observations are consistent with this idea. 1) Frequency response areas of MD cells consist of excitatory and inhibitory domains. MD cells exhibited a higher proportion of multiple excitatory domains and narrower excitatory frequency domains than BD cells, features that may reflect specialization for spectral-dependent directional sensitivity. 2) MD sensitivity requires sound pressure in excitatory and inhibitory frequency domains. Directional sensitivity was evaluated using stimuli with frequency components confined exclusively to excitatory domains (E-only stimuli) or distributed in both excitatory and inhibitory domains (E/I stimuli). Each of 13 MD cells that were tested exhibited higher directional sensitivity to E/I than to E-only stimuli; most MD cells exhibited relatively low directional sensitivity when frequency components were confined exclusively to excitatory domains. 3) MD sensitivity derives from excitatory/inhibitory antagonism (spectral inhibition). Comparison of responses to best frequency and E/I stimuli provided strong support for spectral inhibition. Although spectral facilitation conceivably could contribute to directional sensitivity with direction-dependent increases in response, the results did not show this to be a significant factor. 4) Direction-dependent decreases in responsiveness to BBN reflect increased sound pressure in inhibitory relative to excitatory frequency domains. This idea was tested using the strength of two-tone inhibition, which is a function of stimulus levels in inhibitory relative to excitatory frequency domains. The finding that two-tone inhibition was stronger at directions where BBN responses were minimal than at directions where they were maximal supports the model.

Comparison of noise and tone azimuth tuning of neurons in cat primary auditory cortex and medical geniculate body

1995 ◽  
Vol 74 (3) ◽  
pp. 961-980 ◽  
Author(s):  
J. C. Clarey ◽  
P. Barone ◽  
W. A. Irons ◽  
F. K. Samson ◽  
T. J. Imig
Keyword(s):  
Auditory Cortex ◽  
Medial Geniculate Body ◽  
Primary Auditory Cortex ◽  
Broadband Noise ◽  
Statistical Analyses ◽  
Data Set ◽  
Degree Elevation ◽  
Level Data ◽  
Medial Geniculate ◽  
Ventral Nucleus

1. A comparison of the azimuth tuning of single neurons to broadband noise and to best frequency (BF) tone bursts was made in primary auditory cortex (AI: n = 173) and the medial geniculate body (MGB: n = 52) of barbiturate-anesthetized cats. Observations were largely restricted to cells located within the tonotopically organized divisions of the MGB (i.e., the ventral nucleus and the lateral division of the posterior nuclear group) and the middle layers of AI. All cells studied had BFs > or = 4 kHz. 2. The responses of each cell to sounds presented from seven frontal azimuthal locations (-90 to +90 degrees in 30 degrees steps; 0 degree elevation) and at five sound pressure levels (SPLs: 0-80 dB or 5-85 dB in 20-dB steps) provided an azimuth-level data set. Responses were averaged over SPL to obtain an azimuth function, and a number of features of this function were used to describe azimuth tuning to noise and to tone stimulation. Azimuth function modulation was used to assess azimuth sensitivity, and cells were categorized as sensitive or insensitive depending on whether modulation was > or = 75% or < 75% of maximum, respectively. The majority (88%) of cells in the sample were azimuth sensitive to noise stimulation, and statistical analyses were restricted to these cells, which are presumably best suited to encode sound source azimuth. Azimuth selectivity was assessed by a preferred azimuth range (PAR) over which azimuth function values exceeded 75% (PAR75) or 50% of maximum response. Cells were categorized according to the location and extent of their noise PARs. Unbounded cells had laterally located PARs that extended to the lateral pole (+/- 90 degrees); bounded cells had PARs that were contained entirely within the frontal hemifield, and a subset of these had PARs centered on the midline (+/- 15 degrees). A final group of cells exhibited multipeaked azimuth functions to noise stimulation. 3. Azimuth functions to noise were generally more selective and/or more sensitive than those to tones. Statistical analyses showed that these differences were significant for cells in each azimuth function category, and for the thalamic and cortical samples. With the exception of multipeaked cells, responsiveness to noise was significantly lower than that to tones in all categories, and for the thalamic and cortical samples.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Is GABA neurotransmission enhanced in auditory thalamus relative to inferior colliculus?

2014 ◽  
Vol 111 (2) ◽  
pp. 229-238 ◽  
Author(s):  
Rui Cai ◽  
Bopanna I. Kalappa ◽  
Thomas J. Brozoski ◽  
Lynne L. Ling ◽  
Donald M. Caspary
Keyword(s):  
Inferior Colliculus ◽  
Chloride Channel ◽  
Single Unit ◽  
Ex Vivo ◽  
Medial Geniculate Body ◽  
Gamma Aminobutyric Acid ◽  
Auditory Thalamus ◽  
Medial Geniculate

Gamma-aminobutyric acid (GABA) is the major inhibitory neurotransmitter in the central auditory system. Sensory thalamic structures show high levels of non-desensitizing extrasynaptic GABAA receptors (GABAARs) and a reduction in the redundancy of coded information. The present study compared the inhibitory potency of GABA acting at GABAARs between the inferior colliculus (IC) and the medial geniculate body (MGB) using quantitative in vivo, in vitro, and ex vivo experimental approaches. In vivo single unit studies compared the ability of half maximal inhibitory concentrations of GABA to inhibit sound-evoked temporal responses, and found that GABA was two to three times ( P < 0.01) more potent at suppressing MGB single unit responses than IC unit responses. In vitro whole cell patch-clamp slice recordings were used to demonstrate that gaboxadol, a δ-subunit selective GABAAR agonist, was significantly more potent at evoking tonic inhibitory currents from MGB neurons than IC neurons ( P < 0.01). These electrophysiological findings were supported by an in vitro receptor binding assay which used the picrotoxin analog [3H]TBOB to assess binding in the GABAAR chloride channel. MGB GABAARs had significantly greater total open chloride channel capacity relative to GABAARs in IC ( P < 0.05) as shown by increased total [3H]TBOB binding. Finally, a comparative ex vivo measurement compared endogenous GABA levels and suggested a trend towards higher GABA concentrations in MGB than in IC. Collectively, these studies suggest that, per unit GABA, high affinity extrasynaptic and synaptic GABAARs confer a significant inhibitory GABAAR advantage to MGB neurons relative to IC neurons. This increased GABA sensitivity likely underpins the vital filtering role of auditory thalamus.

Tonotopic organization in lateral part of posterior group of thalamic nuclei in the cat

1985 ◽  
Vol 53 (3) ◽  
pp. 836-851 ◽  
Author(s):  
T. J. Imig ◽  
A. Morel
Keyword(s):  
High Frequency ◽  
Tone Burst ◽  
Lateral Part ◽  
Thalamic Nuclei ◽  
Burst Stimulation ◽  
Tonotopic Organization ◽  
Frequency Representation ◽  
Posterior Group ◽  
Medial Geniculate ◽  
Ventral Nucleus

Responses of single units and clusters of units to tone-burst stimulation were recorded at 100-micron intervals along vertical electrode penetrations through the lateral part of the posterior group of thalamic nuclei (Po) in five barbiturate-anesthetized cats. Best frequencies and minimum response latencies to tone-burst stimulation were studied at each location along a penetration. Most of Po is located rostral to the medial geniculate body (MGB) and is contiguous with the ventral nucleus and medial division. Po is characterized physiologically by narrowly tuned, short-latency (less than 40 ms) responses. Considerable scatter of best frequencies occurs along electrode penetrations, although a clear tonotopic organization is apparent in the distribution of best frequencies obtained from several electrode penetrations located in the same frontal plane of an individual brain. A "single" frequency is represented as an irregularly shaped lamina. A three-dimensional "block" model of the tonotopic organization of Po is described in which the highest best frequencies are located caudally, and the lowest best frequencies are located rostrally within the nucleus. The high-frequency representation of Po is contiguous with the high-frequency representation of the ventral nucleus of the MGB. The low- and middle-frequency representations of the ventral nucleus and Po are discontinuous. The ventral nucleus and Po have similar physiological properties and together constitute the tonotopic division of the auditory thalamus in the cat. Neurons in the medial division adjacent to the medial border of Po are larger than neurons in Po, lack tonotopic organization, and respond at short latencies.

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