scholarly journals Response Properties of Neighboring Neurons in the Auditory Midbrain for Pure-Tone Stimulation: A Tetrode Study

2007 ◽  
Vol 98 (4) ◽  
pp. 2058-2073 ◽  
Author(s):  
Chandran V. Seshagiri ◽  
Bertrand Delgutte

The complex anatomical structure of the central nucleus of the inferior colliculus (ICC), the principal auditory nucleus in the midbrain, may provide the basis for functional organization of auditory information. To investigate this organization, we used tetrodes to record from neighboring neurons in the ICC of anesthetized cats and studied the similarity and difference among the responses of these neurons to pure-tone stimuli using widely used physiological characterizations. Consistent with the tonotopic arrangement of neurons in the ICC and reports of a threshold map, we found a high degree of correlation in the best frequencies (BFs) of neighboring neurons, which were mostly <3 kHz in our sample, and the pure-tone thresholds among neighboring neurons. However, width of frequency tuning, shapes of the frequency response areas, and temporal discharge patterns showed little or no correlation among neighboring neurons. Because the BF and threshold are measured at levels near the threshold and the characteristic frequency (CF), neighboring neurons may receive similar primary inputs tuned to their CF; however, at higher levels, additional inputs from other frequency channels may be recruited, introducing greater variability in the responses. There was also no correlation among neighboring neurons' sensitivity to interaural time differences (ITD) measured with binaural beats. However, the characteristic phases (CPs) of neighboring neurons revealed a significant correlation. Because the CP is related to the neural mechanisms generating the ITD sensitivity, this result is consistent with segregation of inputs to the ICC from the lateral and medial superior olives.

2014 ◽  
Vol 112 (4) ◽  
pp. 981-998 ◽  
Author(s):  
Małgorzata M. Straka ◽  
Samuel Schmitz ◽  
Hubert H. Lim

The central auditory system has traditionally been divided into lemniscal and nonlemniscal pathways leading from the midbrain through the thalamus to the cortex. This view has served as an organizing principle for studying, modeling, and understanding the encoding of sound within the brain. However, there is evidence that the lemniscal pathway could be further divided into at least two subpathways, each potentially coding for sound in different ways. We investigated whether such an interpretation is supported by the spatial distribution of response features in the central nucleus of the inferior colliculus (ICC), the part of the auditory midbrain assigned to the lemniscal pathway. We recorded responses to pure tone stimuli in the ICC of ketamine-xylazine-anesthetized guinea pigs and used three-dimensional brain reconstruction techniques to map the location of the recording sites. Compared with neurons in caudal-and-medial regions within an isofrequency lamina of the ICC, neurons in rostral-and-lateral regions responded with shorter first-spike latencies with less spiking jitter, shorter durations of spiking responses, a higher proportion of spikes occurring near the onset of the stimulus, lower thresholds, and larger local field potentials with shorter latencies. Further analysis revealed two distinct clusters of response features located in either the caudal-and-medial or the rostral-and-lateral parts of the isofrequency laminae of the ICC. Thus we report substantial differences in coding properties in two regions of the ICC that are consistent with the hypothesis that the lemniscal pathway is made up of at least two distinct subpathways from the midbrain up to the cortex.


1988 ◽  
Vol 60 (6) ◽  
pp. 1823-1840 ◽  
Author(s):  
C. E. Schreiner ◽  
G. Langner

1. The topographical distributions of single-unit and multiple-unit responses to amplitude-modulated tones--and to other relevant parameters of simple tonal stimuli--were defined across the main frequency representational gradient and within narrow frequency ranges represented in "frequency band laminae" in the principal midbrain auditory nucleus, the central nucleus of the inferior colliculus (ICC), in adult, barbiturate-anesthetized cats. 2. Responses to amplitude-modulated tones with the carrier set at the characteristic frequency (CF) of recorded neurons were obtained at many ICC locations in each experiment. The best modulation frequency (BMF) of neurons was defined at each site as that modulation frequency producing the highest neural discharge rate. Encountered BMFs ranged from approximately 10 to 1,000 Hz. A significant range of BMFs were recorded for neurons with any given characteristic frequency. BMF ranges varied as a systematic function of CF and of ICC recording depth. 3. Recorded BMFs were distributed topographically within functionally defined ICC frequency band laminae. Highest BMFs were found clustered in an ICC sector roughly between the middle and lateral third of its frequency band laminae. Progressively lower BMFs were recorded with increasing distance across the laminae in any direction away from the highest-BMF cluster. That is, "iso-BMF contours" were arrayed concentrically around the highest-BMF region. 4. Within frequency band laminae centered at approximately 3 and 12 kHz, quality factors (Q10 dBS) of frequency tuning curves were found to be between 0.8 and 8. Q10 dB values were distributed topographically within given frequency band laminae. Responses with narrow tuning curves (high Q10 dB values) were clustered in the middle third of the mediolateral extent of laminae; sharpness of tuning declined systematically away from this focus of highest Q10 dB values. The center of this distribution did not coincide with the center of the BMF distribution within the same lamina. 5. For neurons at greater than 90% of the ICC loci studied in these experiments, onset latencies to CF tones defined approximately 60 dB above response threshold fell within a range between 5 and 18 ms. Across a given frequency band lamina, onset latencies varied systematically, with longest response latencies recorded medially, and progressively shorter latencies recorded progressively more laterally. 6. Binaural interaction types were systematically distributed within frequency-band laminae. A cluster of excitatory-excitatory (EE) was seen, covering approximately one-third of the mapped area.(ABSTRACT TRUNCATED AT 400 WORDS)


1962 ◽  
Vol 40 (1) ◽  
pp. 7-12
Author(s):  
J. M. Langlois ◽  
Guy Lamarche

The projections of the trigeminal nerve in the pontine reticular formation of the cat have been investigated by recording unit activity, after physiological stimulation of the face, in 30 "encéphales isolés" preparations. No somatotopical arrangement was found but a high degree of spatial convergence onto pontine reticular units exists and a certain degree of functional organization was observed.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Aaron Benson Wong ◽  
J Gerard G Borst

The dorsal (DCIC) and lateral cortices (LCIC) of the inferior colliculus are major targets of the auditory and non-auditory cortical areas, suggesting a role in complex multimodal information processing. However, relatively little is known about their functional organization. We utilized in vivo two-photon Ca2+ imaging in awake mice expressing GCaMP6s in GABAergic or non-GABAergic neurons in the IC to investigate their spatial organization. We found different classes of temporal responses, which we confirmed with simultaneous juxtacellular electrophysiology. Both GABAergic and non-GABAergic neurons showed spatial microheterogeneity in their temporal responses. In contrast, a robust, double rostromedial-caudolateral gradient of frequency tuning was conserved between the two groups, and even among the subclasses. This, together with the existence of a subset of neurons sensitive to spontaneous movements, provides functional evidence for redefining the border between DCIC and LCIC.


1995 ◽  
Vol 74 (4) ◽  
pp. 1689-1700 ◽  
Author(s):  
Y. Albeck ◽  
M. Konishi

1. Extracellular single-unit recording in anesthetized barn owls was used to study neuronal response to dichotic stimuli of variable binaural correlation (BC). Recordings were made in the output fibers of nucleus laminaris (NL), the anterior division of the ventral lateral lemniscal nucleus (VLVa), the core of the central nucleus of the inferior colliculus (ICcC), the lateral shell of the central nucleus of the inferior colliculus (ICcLS), and the external nucleus of the inferior colliculus (ICx). 2. The response of all neurons sensitive to interaural time difference (ITD) varied with BC. The relationship between BC and impulse number fits a linear, a parabolic, or a ramp model. A linear or parabolic model fits most neurons in low-level nuclei. Higher order neurons in ICx did not respond to noise bursts with strong negative binaural correlation, creating a ramp-like response to BC. 3. A neuron's ability to detect ITD varied as a function of BC. Conversely, a neuron's response to BC changed with ITD. Neurons in NL, VLVa, and ICcC show almost periodic ITD response curves. In these neurons peaks and troughs of ITD response curves diminished as BC decreased, creating a flat ITD response when BC = 0. When BC was set to -1, the most favorable ITD became the least favorable one and vice versa. The ITD response curve of ICx neurons usually has a single dominant peak. The response of those neurons to a negatively correlated noise pair (BC = -1) showed two ITD peaks, flanking the position of the primary peak. 4. The parabolic BC response of NL neurons fits the prediction of the cross-correlation model, assuming half-wave rectification of the sound by the cochlea. Linear response is not predicted by the model. However, the parabolic and the linear neurons probably do not belong to two distinct groups as the difference between them is not statistically significant. Thus, the cross-correlation model provides a good description of the binaural response not only in NL but also in VLVa and ICcC. 5. Almost all ramp neurons occurred in either ICx or ICcLS where neurons are more broadly tuned to frequency than those in the lower nuclei. The synthesis of this response type requires, however, not only the convergence of different frequency channels but also inhibition between different ITD channels. We modeled the ramp response as a three-step process. First, different spectral channels converge to create broad frequency tuning. The response to variation in BC will be linear (or parabolic) because it is a sum of linear (parabolic) responses. Second, the activity in some adjacent ITD channels is subtracted by lateral inhibition. Finally, the result is rectified using a high threshold to avoid negative activity.


1994 ◽  
Vol 71 (5) ◽  
pp. 1959-1975 ◽  
Author(s):  
B. Tian ◽  
J. P. Rauschecker

1. Single-neuron activity was recorded from the anterior auditory field (AAF) in the cortex of gas-anesthetized cats. 2. Tone bursts and broad-band complex sounds were used for auditory stimulation. Responses to frequency-modulated (FM) sounds, in particular, were studied systematically. 3. Linear FM sweeps were centered around the best frequency (BF) of a neuron and had an excursion large enough to cover its whole frequency tuning range. Rate and direction of change of the FM sweeps were varied. 4. In 69% of the FM responses, a peak was found at an instantaneous frequency that corresponded to the BF in the pure-tone response. Thirty-three percent of the units had multiple maxima in their FM response. These secondary maxima were not always reflected in the pure-tone response of the same neurons. 5. The vast majority of AAF neurons showed one of two types of selectivity for FM rate. Depending on the criterion, almost half of the cells (46%) preferred fast changes of > 200 Hz/ms (high-pass) in both FM directions. Forty-eight percent of all neurons showed band-pass behavior with a clear preference in the middle range of FM rates in one or both directions. Low-pass or all-pass neurons made up only a small proportion (4 and 1%, respectively) of AAF neurons. 6. When both directions of an FM sweep (low-to-high and high-to-low-frequency) were tested, 66% of the neurons clearly were selective for one direction. This selectivity was not present necessarily at the preferred FM rate. In general, FM direction selectivity was most pronounced at slower FM rates. 7. The selectivity of AAF neurons for the rate and direction of FM sounds makes these neurons suitable for the detection and analysis of communication sounds, which often contain FM components with a particular sweep rate and direction.


2004 ◽  
Vol 91 (1) ◽  
pp. 136-151 ◽  
Author(s):  
Sarah M. N. Woolley ◽  
John H. Casseday

The avian mesencephalicus lateralis, dorsalis (MLd) is the auditory midbrain nucleus in which multiple parallel inputs from lower brain stem converge and through which most auditory information passes to reach the forebrain. Auditory processing in the MLd has not been investigated in songbirds. We studied the tuning properties of single MLd neurons in adult male zebra finches. Pure tones were used to examine tonotopy, temporal response patterns, frequency coding, intensity coding, spike latencies, and duration tuning. Most neurons had no spontaneous activity. The tonotopy of MLd is like that of other birds and mammals; characteristic frequencies (CFs) increase in a dorsal to ventral direction. Four major response patterns were found: 1) onset (49% of cells); 2) primary-like (20%); 3) sustained (19%); and 4) primary-like with notch (12%). CFs ranged between 0.9 and 6.1 kHz, matching the zebra finch hearing range and the power spectrum of song. Tuning curves were generally V-shaped, but complex curves, with multiple peaks or noncontiguous excitatory regions, were observed in 22% of cells. Rate-level functions indicated that 51% of nononset cells showed monotonic relationships between spike rate and sound level. Other cells showed low saturation or nonmonotonic responses. Spike latencies ranged from 4 to 40 ms, measured at CF. Spike latencies generally decreased with increasing sound pressure level (SPL), although paradoxical latency shifts were observed in 16% of units. For onset cells, changes in SPL produced smaller latency changes than for cells showing other response types. Results suggest that auditory midbrain neurons may be particularly suited for processing temporally complex signals with a high degree of precision.


2019 ◽  
Vol 93 (1) ◽  
pp. 34-50
Author(s):  
Catherine A. McCormick

The dorsal portion of the descending octaval nucleus (dDO), the main first-order auditory nucleus in jawed fish, includes four lateral and three medial neuronal populations that project to the auditory midbrain. One medial population and one lateral population contain neurons that receive a remarkably large axon terminal from the utricular branch of the octaval nerve. Immunocytochemistry for connexin 35 (Cx35) was used to determine whether this connection includes electrical synapses. Although Cx35 was not localized to these large contacts, it was observed in the three other lateral dDO populations. Another first-order nucleus, the dorsal portion of the anterior octaval nucleus (dAO), primitively projects to the auditory midbrain in jawed fishes and contains neurons positive for Cx35. Utricular branch terminals were coincident with some Cx35 puncta in dDO and dAO. The results are discussed in light of what is known about the occurrence of electrical synapses in first-order auditory and vestibular nuclei in fish and tetrapods.


2006 ◽  
Vol 96 (5) ◽  
pp. 2177-2188 ◽  
Author(s):  
Laura M. Hurley

The neuromodulator serotonin has a complex set of effects on the auditory responses of neurons within the inferior colliculus (IC), a midbrain auditory nucleus that integrates a wide range of inputs from auditory and nonauditory sources. To determine whether activation of different types of serotonin receptors is a source of the variability in serotonergic effects, four selective agonists of serotonin receptors in the serotonin (5-HT) 1 and 5-HT2 families were iontophoretically applied to IC neurons, which were monitored for changes in their responses to auditory stimuli. Different agonists had different effects on neural responses. The 5-HT1A agonist had mixed facilitatory and depressive effects, whereas 5-HT1B and 5-HT2C agonists were both largely facilitatory. Different agonists changed threshold and frequency tuning in ways that reflected their effects on spike count. When pairs of agonists were applied sequentially to the same neurons, selective agonists sometimes affected neurons in ways that were similar to serotonin, but not to other selective agonists tested. Different agonists also differentially affected groups of neurons classified by the shapes of their frequency-tuning curves, with serotonin and the 5-HT1 receptors affecting proportionally more non-V-type neurons relative to the other agonists tested. In all, evidence suggests that the diversity of serotonin receptor subtypes in the IC is likely to account for at least some of the variability of the effects of serotonin and that receptor subtypes fulfill specialized roles in auditory processing.


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